- Top of page
- Materials and methods
1. Carnivore overabundance that results from exploitation of human derived resources can have numerous detrimental effects on local human populations and ecological communities. Experimental studies on the responses of overabundant carnivores to reductions of such resources are necessary to understand the effectiveness and impacts of resource reduction.
2. We conducted controlled experiments in two villages in which we drastically reduced the availability of anthropogenic food sources in half of each village. Spatial and numerical responses of radio-collared red foxes Vulpes vulpes were recorded and contrasted with those of radio-collared foxes in three similar untreated villages and pristine areas in the region. In total, we looked at survival rates of 134 foxes.
3. Prior to the resource manipulation, home range sizes (0·47 and 0·56 km2) and population densities (30 and 36 foxes km−2) in the two villages were comparable to documented low and high-end values, respectively.
4. Fast and distinct spatial responses were observed in response to the resource manipulation, and were manifested in either increased home range size or home range shifts. In one village, foxes exposed to reduced resource availability more than doubled their home range size.
5. Survival rates of individuals in the treated areas were drastically reduced. Actual fox mortality in the two treated areas reached 100% and 64% within 12 months of the onset of resource manipulation. Estimated monthly survival in the two treated areas declined from 0·96–0·98 and 0·98–0·99 (∼0·69 and 0·78 derived annual survival) before treatment to 0·80–0·83 and 0·92–0·94 (∼<0·01 and 0·42 derived annual survival) after treatment, respectively. By contrast, average monthly survivorship in pristine areas was nearly 0·97 (∼0·69 annual survival) and in the untreated areas and other non-treated villages was 0·95–0·99 (∼0·54–0·89 annual survival).
6.Synthesis and applications. This study demonstrates that sound waste disposal measures are very effective in controlling populations of overabundant carnivores. Contrary to common notion, the response of foxes to reduced resources was fast, manifested more by reduced survival than by successful dispersal into adjacent pristine areas. The results offer support to the Resource Dispersion Hypothesis regarding both home range size and density (suggested by the sharp decrease in survival) as a function of the spatial and temporal dispersion of resource.
- Top of page
- Materials and methods
Supported by anthropogenically derived resources, canid densities near human settlements can be as much as 15 times higher than those in pristine areas (Cavallini 1996; Adkins & Scott 1998; Fedriani, Fuller & Sauvajot 2001; Panez & Bresinski 2002). High canid densities can have numerous detrimental effects on local human populations and ecological communities (Sillero-Zubiri & Switzer 2004), including increased livestock depredation and damage to farming infrastructure (Asheim & Mysterud 2004; Michalski et al. 2006; Holmern, Nyahongo & Roskaft 2007), elevated risk of disease outbreaks (Anderson et al. 1981; Daszak, Cunningham & Hyatt 2000; Yakobson 2007), and disruption of trophic cascades (Yom-Tov & Mendelssohn 1988; Dickman 1996; Newton 1998; Saltz et al. 2002). As invasive species, carnivores when uncontrolled can pose a substantial threat to native species, driving many to extinction (Saunders et al. 1995; Dickman 1996). Consequently, the management and control of carnivores in human-dominated landscapes is of major concern (Treves & Karanyh 2003; Sillero-Zubiri & Switzer 2004) for both economic and conservation reasons. However, active reduction of canid densities by shooting or poisoning commonly raises public objections and is often ineffective due to the high recruitment rates of canids, their nocturnal behaviour, and lack of species specificity (Sillero-Zubiri & Switzer 2004). Improved sanitation procedures, on the other hand, are considered to be effective only in the long-term as a result of an assumed delayed response. This has raised concerns over the possibility of individuals from a treated area spilling over into the surrounding natural environment and causing a ‘crowding the ark’ effect (Meffe & Carroll 1997). To date, studies examining carnivore responses to reduced resources have sought correlations between relevant variables (Baker 2000; Gilchrist & Otali 2002; Johnson et al. 2002; Pereira, Fracassi & Uhart 2006), so that planned experimental studies on the responses of overabundant carnivores to resource reduction remain to be done.
Israel’s Galilee and northern periphery is characterized by a large number of small villages that rely economically on family farms. Often, these villages lack any organized means of husbandry waste disposal, and carcasses from poultry cultivation and other wastes are dumped in the open. As a result, these villages are transformed into hotspots for many wild canids, mainly the red fox Vulpes vulpes and golden jackal Canis aureus (Dolev et al. 2004; Dolev 2006), both native to the region. Existing conditions offer a unique opportunity to study the responses of canids when improved sanitation procedures are implemented.
In this work, we examined the short-term effects of reducing anthropogenic resources on foxes scavenging near poultry farms in two Israeli villages by eliminating poultry carcasses. We contrasted the survival and spatial responses of foxes to the sudden decrease in anthropogenic resources with those of foxes in three untreated villages and in the region’s pristine areas. We focused our study on fox survival and spatial responses to the sudden decrease in resources.
- Top of page
- Materials and methods
In total, we radio-collared 134 foxes (74 females, 60 males). In KS, we radio-collared 17 foxes (10 females, 7 males). In KH we radio-collared 18 foxes (11 females, 7 males). In a previous study (Dolev 2006), we radio-collared: KS – 28 foxes (15 females, 13 males), Shefer – 6 foxes (1 female, 5 males), Parod – 5 foxes (3 females, 2 males), Hazon – 17 foxes (11 females, 6 males) and in the pristine regions – 43 foxes (23 females, 20 males).
At the time of the resource manipulation, nine foxes were present in the treated area of KS and six in the untreated area. By the end of 6 months, eight foxes had perished in the treated area (i.e. mortality of 89%). In the untreated area only one was found dead and another’s signal was lost. After 12 months, all foxes (100%) had perished in the treated area, contrasting with only three (50%) in the untreated area. In KH, 11 foxes were subjected to the resource manipulation. Only five foxes (55%) survived after 6 months and four (64%) after 12 months. In the untreated area, five adult foxes were present at the onset of the resource manipulation with four (i.e. mortality of 20%) surviving after 6 months and three (40%) after 12 months.
All the leading models using the known-fates module in MARK included the treatment effect (Table 1). Three models had substantial support (QAICc < 2·0) and included, other than the treatment, a site effect (labelled ‘p.sites’ in Table 1) with all eight groups, a season effect (one model) and a sex effect (one model). Evidence ratios for these three leading models compared to their counterpart without the treatment effect were >40,000:1 (model 1 vs. 24), >38,000:1 (model 2 vs. 25), and 9,000:1 (model 3 vs. 28). Models with all untreated areas grouped together (termed ‘v.sites’ in Table 1) had lesser support.
Monthly survival estimates per season dropped in the treated area in KS from ∼0·97 before treatment to 0·80–0·83 (Table 2) and in KH from 0·98–0·99 to 0·92–0·94. This amounts to an annual decline in survivorship from 0·69 to <0·01 in KS and from 0·78 to 0·42 in KH. Seasonal survivorship in the natural areas ranged from 0·95 to 0·97. Monthly survival in all villages (including the pre-treatment values for the treatment areas in KS and KH) was as much as 0·99, except in Hazon where it ranged from 0·96 to 0·94.
Table 2. Estimated monthly survival rates per season (S – spring, A – autumn, and W – winter) for each of the areas, stratified by gender. Treated periods are highlighted in grey.
|KS ♀||KS ♂||KS.T ♀||KS.T ♂||KH ♀||KH ♂||KH.T ♀||KH.T ♂||Parod ♀||Parod ♂||Shefer ♀||Shefer ♂||Hazon ♀||Hazon ♂||Pristine ♀||Pristine ♂|
|2002||S||0·97|| || || || || || || ||0·97|| || ||0·99|| || || || |
|2002||A||0·98|| || || || || || || ||0·98|| || ||0·99|| || ||0·97|| |
|2003||W||0·98|| || || || || || || ||0·98|| ||0·99||0·99|| || ||0·97|| |
|2003||S||0·97|| || || || || || || ||0·97||0·97||0·99||0·99|| || ||0·97|| |
|2003||A||0·97|| ||0·97|| || || || || ||0·98||0·98||0·99||0·99|| || ||0·97|| |
|2004||W||0·98||0·98||0·98|| || || || || ||0·98||0·98||0·99||0·99|| || ||0·97||0·97|
|2004||S||0·97||0·97||0·97|| || || || || ||0·97||0·97|| ||0·98||0·94||0·94||0·96||0·96|
|2004||A||0·97||0·97||0·97|| || || || || ||0·98||0·97|| ||0·99||0·95||0·95||0·97||0·97|
|2005||W||0·97||0·97||0·97|| || || || || || ||0·98|| ||0·99||0·95||0·95||0·97||0·97|
|2005||S||0·97||0·97||0·97|| || || || || || || || ||0·99||0·95||0·94||0·97||0·97|
|2005||A||0·98||0·97||0·98|| || || || || || || || ||0·99||0·95||0·95||0·97|| |
|2006||W||0·98||0·98||0·98|| || || || || || || || ||0·99||0·96||0·96||0·97||0·97|
|2006||S||0·96||0·96||0·96||0·96|| || || || || || || ||0·98||0·94||0·94||0·96||0·96|
|2006||A|| ||0·97||0·97||0·97|| || || || || || || ||0·98||0·95||0·95||0·97||0·97|
|2007||W||0·97||0·97||0·83||0·83|| || || || || || || ||0·99||0·95|| ||0·97|| |
|2007||S||0·97||0·97||0·80||0·80||0·98||0·98||0·98||0·98|| || || ||0·98||0·94|| ||0·96|| |
|2007||A|| ||0·97|| || ||0·99||0·99||0·99||0·99|| || || ||0·99|| || ||0·97|| |
|2008||W||0·98||0·97|| || ||0·99||0·99||0·93||0·93|| || || ||0·99|| || ||0·97|| |
|2008||S||0·97||0·97|| || ||0·99||0·99||0·93||0·92|| || || ||0·99|| || ||0·97|| |
|2008||A||0·98||0·97|| || ||0·99||0·99||0·94||0·94|| || || ||0·99|| || ||0·97|| |
|2009||W||0·98||0·98|| || ||0·99||0·99||0·94||0·94|| || || ||0·99|| || ||0·97|| |
|2009||S||0·97||0·97|| || ||0·99||0·99||0·94||0·94|| || || ||0·99|| || ||0·97|| |
Home range size
In KS, 1128 and 605 telemetry locations were recorded in the pre- and post-manipulation periods, respectively. Average telemetry locations per animal were 64 ± 24. Prior to the manipulation, average fox home range size in KS was 0·47 km2 ± 0·25 (n = 17). The slope of change in home range size from the start of the manipulation using the MWK procedure showed significant differences in the rates at which home range size increased between foxes from the two sides of the village (t = 6·97, df = 9, P < 0·001). Home range size of southern foxes more than doubled to an average of 1·2 km2 ± 0·35 (n = 3). In KH, 169 and 258 telemetry locations were recorded in the pre- and post-manipulation periods, respectively, with 25 ± 13 locations per animal. Pre-manipulation average fox home range size was 0·56 km2 ± 0·41 (n = 12). A significant increase in home range size was observed in both sides of the village in the post-manipulation period (North: χ2 = 17·87, df = 6, P = 0·007, South: χ2 = 51·84, df = 18, P < 0·001).
Linear regression slopes obtained through the MWK procedure, showed that the centroid of activity of foxes in the southern part of KS moved away from the manipulation area. Distance from the manipulation area increased for animals foraging in the southern part of the village from 28 m prior to the manipulation to 136 m in the months following (t = −21·23, df = 2, P = 0·002). By contrast, the distance of the centroid of activity of animals foraging in the northern part of the village remained unchanged (t = −1·40, df = 6, P = 0·21). Recorded location ratios for foxes exposed to the resource manipulation in KH increased significantly towards the northern side of the village in the post-manipulation period in comparison to the pre-manipulation period (t = −2·46, df = 9, P = 0·036). No significant changes were observed in fox location ratios in the unmanipulated area (t = −0·99, df = 2, P = 0·43). Telemetry surveillance over 7 years prior to the resource manipulation revealed foraging distances of only several hundred metres from original capture sites. Long range forays and dispersal – defined as locations outside average home range size boundaries +20%– (3·6 km) (Dolev 2006) – were rare events (0·5%). All long distance movements were confined to foxes moving from the villages to neighbouring natural habitat. As pristine locations were distant from investigated villages, we recorded no cases of long range movements of foxes into treated villages.
- Top of page
- Materials and methods
Increased food availability from human waste can have a profound effect on the reproductive success (Lewis, Sallee & Golightly 1999; Reichmann & Saltz 2005) and densities of wild canids (Panez & Bresinski 2002; Dolev 2006). Prior to our manipulation, the maximum numbers of collared foxes located within the boundaries of the treated villages in one night were 14 in KS and 18 in KH. Given the size of the villages this would translate to an estimated density of 30 and 36 foxes km−2, respectively, within the village areas. These values are at the extreme of previously reported densities for foxes (Macdonald & Reynolds 2005). In addition, sightings of uncollared animals were frequent and, therefore, the above estimates represent an underestimate of the true numbers of foxes within the villages.
The sanitation procedures we applied in both cases reduced available organic refuse and resulted in rapid demographic and behavioural changes in foxes. Responses were manifested in reduced survival rates, changes in home range size, and spatial shifts in home ranges. A cause-and-effect relationship between the availability of food resources and these patterns was established through comparison with individuals residing in the unmanipulated area combined with a temporal comparison to the pre-manipulation patterns in both the manipulated and unmanipulated areas as well as survival rates in other villages and more pristine areas.
Predator populations are expected to respond to changes in prey availability either functionally, i.e. by switching to alternative prey (Angerbjorn, Tannerfeldt & Erlinge 1999), and/or numerically, i.e. via increased mortality (Fuller & Sievert 2001), reduced reproductive success, and reduced immigration and emigration. To date, studies of predators addressing demographic changes in response to declining food availability provide only circumstantial evidence and involve mainly seasonal variation in resources (Pereira et al. 2006).
Average annual survival probability of 77 foxes collared in northern Israel was estimated to be 45·5% during an 18-month period (Dolev 2006). Dolev (2006) further suggested that sub-adult foxes foraging in the vicinity of villages and poultry farms had a slightly higher survival probability compared to that of foxes foraging in natural areas. Our results provide further support for this observation. Thus, the low survival of the animals foraging in the treated sections is notable. The spatial response of the southern foxes to the treatments, either away from the village into the more natural and agricultural areas or to the northern part of the village, suggests these animals might have attempted to establish new foraging grounds and in doing so may have encountered strong intra-specific competition with individuals having a ‘home court advantage.’ Thus, mortality may have been caused by elevated stress resulting from functioning in a less familiar (and thus unpredictable) environment and frequent aggressive interactions, both leading to higher probability of starvation.
It certain cases animals subjected to the resource manipulation dispersed (as opposed to just shifting foraging grounds) to distant, unknown areas. Dispersal has several associated costs, such as increased energy demands, difficulty in finding prey in unfamiliar areas and lack of suitable cover (Woollard & Harris 1990; Koopman, Cypher & Scrivner 2000). Several studies of the red fox have shown that philopatric juveniles generally have higher survival than dispersing juveniles (Harris & Trewhella 1988; Lindstrom 1989; Woollard & Harris 1990). In the case of animals in the manipulated areas, both home range size and the foraging locations changed as a result of the resource manipulation. However, even if the daytime resting site locations remained unchanged (i.e. animals did not disperse), the energy expenditure involved in shifting foraging grounds away from these areas could be excessive.
According to the Resource Dispersion Hypothesis (RDH) (Macdonald 1983), when resources are clumped in space and/or in time, the economics of exploiting these patches enables several individuals to share resources over a common area, satisfying their resource needs without imposing large costs on each other (Johnson et al. 2002), but see Revilla (2003) and Johnson et al. (2003). Although several studies support the RDH (Johnson et al. 2002), the strongest test for the RDH would be through controlled experiments. Surprisingly, we found no designed studies investigating alterations in food availability and its effect on behavioural responses of carnivores (Johnson et al. 2002). The literature examining carnivore responses addresses this issue only by finding predicted correlations between the relevant variables (Baker 2000; Gilchrist & Otali 2002; Johnson et al. 2002; Pereira et al. 2006). The results of this study corroborate the RDH predictions regarding both home range size and density (suggested by the sharp decrease in survival) as a function of the spatial and temporal dispersion of resources (Macdonald 1983; Johnson et al. 2002). The pre-manipulation home range sizes and implied densities were comparable to documented low and high-end values, respectively (Macdonald & Reynolds 2005). This is in line with the high spatial concentration of food patches along with high patch richness and predictability in the study area. Prior to the manipulation, animals’ energetic requirements were met within a small territory. Moreover, the high overlap in fox home ranges, while foraging within the village, suggests a reduced pressure on territoriality by animals and the sharing of foraging grounds. According to the RDH, the spatial distribution of resources may explain both positive and negative deviations by social canids from the home range predicted by their metabolic requirements (McNab 1963; Macdonald & Sillero-Zubiri 2004). Average adult fox weights in KS and KH [4·9 and 4·1 kg for males (n = 18) and females (n = 18), respectively] were relatively low for foxes (Macdonald & Reynolds 2005). Along with small home range sizes (and high fox density), our results provide positive affirmation to the allometric relationship (McNab 1963).
As noted in previous studies (Doncaster & Macdonald 1991), the flexible spatial organization of the red fox allows individuals to adapt their home range in light of variation in resource availability. When faced with declining resources in the southern parts of KS and KH, foxes as central place foragers would have two alternatives if they were to maintain their den/day-time shelter while upholding needed energy requirements: forage more in the natural and agricultural landscapes, thus dictating larger dispersion and heterogeneity of patch resources, or forage at longer distances from the den/day-time shelter by venturing into the northern part of the villages (Meia & Weber 1993; Lucherini, Lovari & Crema 1995). In both cases home range is expected to increase and/or shift, as supported herein.
Our results demonstrate that improved sanitation is highly effective in controlling overabundant canids, with rapid changes in their dynamics manifested mostly by reduced survival rather than successful dispersal into adjacent pristine areas. The conflict of overabundant carnivores with humans due to agricultural (Sillero-Zubiri & Switzer 2004; Holmern, Nyahongo & Roskaft 2007), epidemiological (Anderson et al. 1981; Yakobson 2007), and environmental concerns (Dickman 1996; Saltz et al. 2002; Clark et al. 2005) necessitates management (Mendelssohn 1972; Yom-Tov, Ashkenazi & Viner 1995; Nemtzov & King 2002). Carnivore control has been practiced for centuries (Reynolds & Tapper 1996). Nevertheless, active reduction of overabundant predators by poisoning or shooting, although still widely practiced (Saunders et al. 1995; Treves & Karanyh 2003), is subject to public and professional debate. On the one hand, while labour-intensive shooting is species-specific, it is often ineffective (Baker & Harris 2006). On the other hand, cost-effective poisoning can cause indiscriminate eradication of non-target species (Sillero-Zubiri & Switzer 2004). Reducing available anthropogenic resources through improved sanitation, recognized as a solution tackling the problem at its source, has been considered a long-term process with delayed results, i.e. numerical responses might be lagged and can be preceded by overexploitation of the surrounding resources (Fuller & Sievert 2001). However, our findings suggest that improved sanitation is highly effective in controlling overabundant foxes, with rapid changes in their dynamics manifested more by reduced survival than by successful dispersal into adjacent pristine areas. Moreover, reduction of anthropogenic resources had little consequence for lower trophic levels of fauna (Ben-Zvi 2010). Our results support the use of sanitation as a key protocol for managing problematic predator populations (Fedriani et al. 2001; Nyhus & Tilson 2004; Swarner 2004; Peirce & Van Daele 2006). The application of this study to invasive species may be more complex if the increasing abundance of a carnivore species is not attributed solely to human subsidies or livestock depredation. Nonetheless, eliminating access of invasive animals to open landfills and improved husbandry protection and sanitation will inevitably have an adverse effect on their populations. Finally, although not addressed specifically in this study, the changes in abundance of canids in and around the treated villages were noticed by farmers themselves and have encouraged them to maintain a higher level of sanitation after the study was terminated.