ANIMAL BEHAVIOUR, 2006, 71, 577–584 doi:10.1016/j.anbehav.2005.05.022 Behavioural responses of red foxes to an increase in the presence of golden jackals: a field experiment SHANI SCHEININ*,YORAMYOM-TOV*,UZIMOTRO† &ELIGEFFEN* *Department of Zoology, Tel Aviv University yDepartment of Evolution, Systematics and Ecology, and Department of Statistics, The Hebrew University of Jerusalem (Received 22 December 2004; initial acceptance 1 April 2005; final acceptance 19 May 2005; published online 13 February 2006; MS. number: 8411R) The golden jackal, Canis aureus, and the red fox, Vulpes vulpes, are two common canids in Israel. Although the two species have similar diets, the jackal is about three times larger than the red fox. The current evidence for interspecific competition between these two canids is circumstantial and indirect. In this study we aimed to measure experimentally the response of red foxes to increasing exposure to the presence of the golden jackal. Our field experiments comprised three stimuli: urine as a scent stimulus, a mounted specimen and urine as a static animal-image stimulus, and a caged pet animal as a live animal stimulus. The treatment and control were placed near food trays, and the behaviour of foxes around these trays was documented by video recorders. In most cases, the presence of scent or cast of a golden jackal did not alter the behaviour of the foxes. However, foxes avoided the test arena when a live jackal was present. This finding provides strong evidence that red foxes fear jackals, and shows that foxes are more concerned when a live jackal is present. The possible implications of the observed fox behaviour for the understand- ing of large-scale competitive exclusion among canid species are discussed. Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. The Gause principle states that two species with identical accidental removal of one carnivore species had a signifi- ecological demands cannot coexist, and one of them will cant effect on other species of predators. For example, be outcompeted by the other (Gause 1934; Schoener the removal of the grey wolf, Canis lupus, from large areas 1982). Thus, it is generally assumed that closely related in North America was followed by an increase in coyote, sympatric species compete, and the fitness of at least Canis latrans, populations (Peterson 1995), the removal one of the competitors will be negatively affected (Krebs of coyotes was related to changes in populations of other 2001). Hutchinson (1959) suggested that the frequently carnivores in these areas (Henke & Bryant 1999), and a de- observed constant size ratio between species in a feeding cline in populations of the red fox in Scandinavia was fol- guild is a result of such interspecific competition, and it re- lowed by an increase in the population of the pine duces competition by resource partitioning. However, re- marten, Martes martes (Lindstrom et al. 1995). Stealing of source partitioning is rarely complete, and species within prey by larger or more numerous carnivores is a common a feeding guild frequently compete with each other to phenomenon frequently observed in Africa. For example, a certain degree. Within a predator guild, such competi- African hunting dogs, Lycaon pictus (Cooper 1991; Car- tion may take the form of intraguild predation (Holt & Po- bone et al. 1997), and cheetahs, Acinonyx jubatus, often lis 1997) and a recent review shows that predation is lose their prey to lions, Panthera leo, and spotted hyaenas, common (Palomares & Caro 1999). Controlled experi- Crocuta crocuta (Creel & Creel 1996; Vucetich & Creel ments are rare, but several studies have shown that 1999). Potential competitors may avoid each other, as do genets, Genetta genetta, and Egyptian mongooses, Herpestes ichneumon, in the presence of the Iberian lynx, Lynx par- Correspondence: E. Geffen, Department of Zoology, Tel Aviv University, dina (Palomares et al. 1995), and South American grey Tel Aviv 69978, Israel (email: [email protected]). U. Motro is at foxes, Dusicyon griseus, avoid their congeneric competi- the Department of Evolution, Systematics and Ecology, and Department tors, D. culpaeus (Johnson & Franklin 1994). However, in- of Statistics, The Hebrew University of Jerusalem, Jerusalem 91904, teractions between two competing species may take Israel. various forms, ranging from tolerance to predation, as 577 0003–3472/05/$30.00/0 Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 578 ANIMAL BEHAVIOUR, 71,3 seen in coyotes and red foxes, Vulpes vulpes (Gese et al. stimulus) and the stimulus of red fox. Lack of a behav- 1996) and in wolves and coyotes (Thurber et al. 1992; ioural response between fox and jackal stimuli would Peterson 1995). suggest that the red foxes in the field view a jackal as Most research on interspecific competition deals with another individual fox and not as a larger predator. On the resource competition within a guild, but studies on other hand, stressful response to the jackal stimulus, predator guilds, including canids (Canidae), deal also relative to the fox stimulus, would imply that foxes view with interference competition (Diamond 1978). Interfer- the jackal as a potential predator or competitor. ence competition, including killing or competitive exclu- sion of one species by another (generally the smaller by the larger), has been described for several canid guilds. METHODS For example, Arctic foxes, Alopex lagopus, were excluded by red foxes (Elmhagen et al. 2002), red foxes by coyotes Study Area (Voigt & Earle 1983; Harrison et al. 1989), and coyotes The study was based on five sites, where the local red by wolves (Thurber et al. 1992). foxes frequently fed and were habituated to the equip- Avoidance behaviour by smaller species seems to be ment used in the experiments (see below). These feeding common. For example, survival rates of coyotes in Alaska sites were situated in the northern Arava Valley (30 460N, were higher where they avoided wolves (Thurber et al. 35 180E), between two villages (Hatzeva and En Yahav) 1992), and red foxes in Maine and Dakota were rarely pre- 12 km apart. To minimize the possibility that individual dated upon by sympatric coyotes, apparently because of foxes from one site would visit another site in the same ex- avoidance (Sargeant et al. 1987; Harrison et al. 1989). In- perimental session, we set up two feeding sites at opposite deed, interaction between two potentially competing spe- ends of each village, and a fifth between the villages. We cies does not have to involve aggression, especially during selected sites where human activity is rare to minimize in- periods of high food availability or when the competitors terference during the experiments. A permit for this re- specialize on different foods (Theberge & Wedeles 1989; search was granted by the Nature and Parks Authority of Paquet 1992; Gese et al. 1996). Israel. The canid guild in Israel is composed of five species: the The study area is an extreme desert. Precipitation wolf, the golden jackal, Canis aureus, and three species of averages 42 mm/year, and most rainfall is restricted to foxes, genus Vulpes. Dayan et al. (1992) found a constant the few thunderstorms that occur in this area during No- size ratio in the carnassials of these species, and claimed vember–February. Mean summer and winter temperatures that this ratio indicates interspecific competition. The are 38 C and 22 C, respectively (Bitan & Rubin 1994). golden jackal and the red fox are common canids in Israel, During the night, temperature drops considerably. Iso- where they feed on a large variety of animal and plant lated trees (Acacia tortilis, Acacia raddiana, Tamarix aphylla) food, as well as being commensal with people. Both spe- and small bushes (Anabasis articulata, Hammada salicorn- cies have been studied in Israel (Golani & Keller 1974; ica, Haloxylon persicum) along creekbeds dominate the Macdonald 1979a; Assa 1990) and elsewhere. They are flat scenery, a set-up of wide visibility. Golden jackals are known to use olfactory marking in their home ranges or rare in this area, but red foxes are abundant. territories, using faeces, urine or secretions from various skin glands (summarized in Mendelssohn & Yom-Tov 1999). The red fox is smaller than the golden jackal Experimental Design (mean body weight 2.6 and 8.5 kg, respectively), and when jackals became very abundant, population size of We conducted each trial by placing in the field a pair of foxes decreased significantly in such areas, apparently be- plastic trays (60 Â 40 cm and 15 cm deep) filled with local cause of exclusion by jackals (Ilani 1979; Mendelssohn & gravel and fox bait for 4 h. We used local gravel to reduce Yom-Tov 1999). However, only anecdotal observations of alien factors (e.g. strange smells) that might interfere with red foxes being chased by jackals are available (Ilani & our treatments. For bait we obtained dead frozen chicks Shalmon 1985; Macdonald 1987). A study of the diet of from the Tel Aviv University Zoo. These chicks are used these two species in Hungary revealed no differences for animal feed and supplied dead to the zoo by breeders. (Lanszki & Heltai 2002), and Kingdon (1997) claimed Five thawed chicks were placed in each tray, one at each that in North Africa golden jackals are more numerous corner and one in the centre, and covered with gravel. than red foxes, apparently because of the inferior position Thus, for each pair of trays we used 10 chicks, about of the foxes in the food hierarchy. 400 g, which is the daily requirement of one 3.5-kg fox Most evidence for interspecific competition between (Macdonald & Barrett 1993). We anticipated that this carnivores is circumstantial and indirect, and as far as we quantity would be an incentive, and not a surfeit, for know there is little experimental evidence on how foxes to participate in our experiment.