ARTICLE IN PRESS

Journal of Arid Environments Journal of Arid Environments 57 (2004) 45–60 www.elsevier.com/locate/jnlabr/yjare

Ecology, diet and behaviour of two species in a large, fenced protected area in central

Daniel M. Lenaina,b, Ernst Olfermanna, Stuart Warringtonb,* a National Wildlife Research Center, P.O. Box 1086, Taif, Saudi Arabia b Department of Environmental Sciences, University of Hertfordshire, Hatfield, Hertfordshire AL10 9AB, UK

Received 1 October 2002; accepted 9 May 2003

Abstract

The aim of the research was to determine the status and to study aspects of the ecology of the fox species Vulpes vulpes arabica and Vulpes ruppelli. sabea inside and outside a large fenced Protected Area, Mahazat as-Sayd in Saudi Arabia. V. ruppelli. sabea was the most abundant small carnivore, witha density of 0.7–1.0 km 2 which was about 12 times greater than V. vulpes arabica and both fox populations were greater inside Mahazat than outside. Annual survivorship of V. ruppelli. sabea was 39% (based on Jolly–Seber method) and 70% (based on mean residence rate). The fox species had similar diets with small and invertebrates being the most important components. V. ruppelli. sabea population existed as pairs holding home ranges all year of 7.2 km2 and producing 3.3 cubs on average. r 2003 Elsevier Ltd. All rights reserved.

Keywords: Fox; Carnivore; Arid; ; Home range; Population ecology; Diet; Mark–release–recapture

1. Introduction

The Vulpes genus is one of the most successful of the Order . However, limited information is available about the status and ecology of in arid and semi-desert areas suchas theArabian Peninsula ( Ginsberg and Macdonald, 1990).

*Corresponding author. E-mail address: [email protected] (S. Warrington).

0140-1963/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0140-1963(03)00088-0 ARTICLE IN PRESS

46 D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60

Three Vulpes species have been recorded in Saudi Arabia. Ruppell’s. fox (Vulpes ruppelli. sabea) and the Arabian (Vulpes vulpes arabica) are the most abundant and widespread (Harrison and Bates, 1991) withBlandford’s fox ( Vulpes cana) being confined to rocky, mountainous areas (Geffen et al., 1992b). In recognition of declining numbers of many species, due to hunting, disturbance and habitat degradation, His Royal Highness Prince Saud Al Faisal established the National Commission for Wildlife Conservation and Development (NCWCD) and the National Wildlife Research Center (NWRC) in Saudi Arabia in 1986. The basis of the Saudi Arabian conservation programme was the NCWCD’s Protected Area System Plan (Child and Grainger, 1990) which established a network of 11 large Protected Areas. The Protected Area Mahazat as-Sayd, established in central-west Saudi Arabia, is unique as it is the only reserve that is fenced. This large area of 2244 km2 provided an opportunity to study the recovery of an arid ecosystem now protected from grazing domestic stock and human disturbance and to evaluate re- introduction programmes that could be used later to release within the wider network of protected areas. Re-introduction programmes at Mahazat as-Sayd have included houbara bustard (Chlamydotis [undulata] macqueenii)(Seddon et al., 1995), Reem Gazelle (Gazella subguttorosa) and Arabian oryx (Oryx leucoryx) (Ostrowski et al., 1998). Six small carnivore species have been recorded in Mahazat as-Sayd (Table 1) including two fox species, Vulpes ruppelli. sabea and V. vulpes arabica. The fox species, especially V. vulpes arabica, have been implicated in adversely affecting the houbara bustard re-introduction programme, with over 40% of deaths of newly released sub-adult attributed to mammalian predators in 1992–94, but avian predators were also a cause of mortality (Combreau and Smith, 1998). There is a very limited literature on the ecology of these fox species in semi-arid areas and only one study of V. ruppelli. sabea which was conducted in (Lindsay and Macdonald, 1986).

Table 1 Small mammalian carnivores of Mahazat as-Sayd, Saudi Arabia

Species Common name Status

Canidae Vulpes vulpes arabica Thomas, 1902 Arabian red fox Common Vulpes ruppelli. sabea Pocock, 1934 Ruppell’s. fox Numerous

Mustelidae Mellivora capensis (Schreber, 1776) Ratel Very rare

Felidae Felis silvestris tristrami Pocock, 1944 African wild cat Occasional Felis margarita harrisoni Hemmer, Grubb and Groves, 1976 Arabian sand cat Occasional Felis domesticus (Linnaeus, 1758) Feral cat Rare

Status in Mahazat is based on this study and observations by NWRC staff. ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 47

The aim of this project was to determine the status and to study aspects of the ecology of fox populations inside and outside the Mahazat as-Sayd Protected Area. The fox population studies were based on intensive mark–release–recapture (MRR) techniques, with some radio-tracking work to research home range and faecal analysis for diet investigations. The results of the study are intended to provide a quantitative basis for the formulation of management plans in Mahazat as-Sayd and other arid region protected areas to ensure that the conservation of native small carnivores and the restoration of potential prey species are complementary endeavours. For example, translocation of foxes away from a houbara release area had not proved to be a cost-effective approach to reducing predation (Lenain and Warrington, 2001). In addition, this is the first extensive study of the ecology of these two fox species in the central plateau of the .

2. The study site, Mahazat as-Sayd

The 2244 km2 Mahazat as-Sayd was declared a Protected Area in 1988 and was surrounded by about 220 km of chainlink fence, topped with barbed wire to a height of 2.1 m by March 1989. The approximate centre of the area is located at 22150N, 41400E, some 150 km north-east of the city of Taif. Mahazat as-Sayd is a hot and semi-arid to arid desert steppe habitat, typical of the central plateau of the Arabian Peninsula, gently undulating at elevations of 900–1050 m above sea level. Three distinct substrates could be distinguished from a 1995 LANDSAT image; a gravel plain, a basalt undulating plain, and a chert area interspersed with basaltic outcrops. Sand and fine gravel are the dominant surface substrates covering over 95% of the Area. Mean monthly maximum temperatures range from 19Cto42C and minimums from 6Cto25C. Rainfall is very variable ranging from 46 to 240 mm per annum over the study period, with an average of 100 mm, and typically occurs between Marchto May eachyear, but withoccasional important rain events at other times. There is no permanent source of water above ground level in Mahazat as-Sayd but ephemeral pools exist for short periods after heavy rain. After completion of the fence 112 vascular plant species were identified, this figure had increased to 142 species by 1994 and 156 species by 1997 (Collenette, 1997). 16 species have been recorded and 159 species of birds, of which 17 have been confirmed as breeding.

3. Methods

The investigations into fox ecology in Mahazat were divided into two phases: (1) an intensive study from May 1992 to January 1994 of foxes in 100 km2 (about 5%) of Mahazat including detailed observation of individual foxes, and (2) a more extensive study from September 1996 to April 1998 across the whole of Mahazat including three sites outside of Mahazat (see Fig. 1). For the purposes of the study, the seasons ARTICLE IN PRESS

48 D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60

Motorway to Riyadh 670 km

To Taif 160 km N

0 20 km

Fig. 1. The fenced Protected Area of Mahazat as-Sayd in central Saudi Arabia. The rectangular box is the trapped area for Phase 1 of the research. indicates the location of a trapping grid from Phase 2 inside Mahazat. J indicate the location of trapping grids outside of Mahazat. The two research camps and the location of gates in the fence are also shown. were defined as: Spring (March–May), Summer (June–August), Autumn (Septem- ber–November), Winter (December–February).

3.1. Population studies

Investigations into fox population abundance were based on mark–release– recapture (MRR) techniques. Tomohawk live traps (Tomohawk Live Trap Company, Wisconsin, USA) of 40 40 108 cm in size were used, and although double ended, only one door was opened. The other end was baited with a piece of raw chicken and was rebaited after 2 days or if the bait had been consumed. The traps have a metal plate, which rises when the trap is set and when tripped causes the door to close. Traps were set and baited in the 2 h before dusk and each trap was placed by vegetation where it would be shaded from the morning sun. Traps were visited within 3 h of first light and all foxes trapped were individually marked using numbered plastic ear tags (Rototags, Dalton Supplies Ltd., UK). All animals on capture or recapture were identified, sexed, weighed to the nearest 10 g and released at the point of capture. The trapping procedures were as follows: Phase 1. Fifty-two traps were established in a 13 4 grid, trap spacing 1 km, and 12 trapping sessions of 10 nights in length were carried out at 45 day intervals. Phase 2. Twelve random points (all more than 2 km from the fence and 10 km from each other) were located across Mahazat and were the centre of the trapping grids. Eachtrapping grid consisted of 10 traps (2 5 grid, trap spacing 1 km). Six ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 49 trapping sessions, of four nights length were carried out over 18 months at about 3 monthintervals. Four trapping grids (40 traps) were set at one time and the12 grids were trapped in three consecutive weeks. Three sites outside of Mahazat were also investigated, but due to the distances to the sites and the need to remain close to the traps to prevent human interference, only 20 traps could be managed at one time and could only be used for two consecutive nights.

3.2. Population estimates

The mark–release–recapture (MRR) technique was used to estimate the population abundance of foxes. If an individual fox was captured more than once within a trapping session (2, 4 or 10-day period), then the data were treated as a single capture/recapture event. A direct enumeration method, the minimum number alive (MNA), can be used when the number of captures and recaptures are too low for population models based on MRR (Nichols and Pollock, 1983). The MNA is based on all animals caught in a session plus those caught previously but not caught in the particular session, but which reappeared in a later session. The population model of Jolly–Seber is the method of choice for open populations (Greenwood, 1996) and was used in this study as recruitment may occur and indeed dispersal (see Lenain and Warrington, 2001). This method requires multiple capture– recapture events and allows for gains and losses, and provides estimates of the addition and survival rates. There are a number of assumptions that need to be met to allow the Jolly–Seber model to be used effectively, including that every individual in the population has an equal chance of capture. The Leslie, Chitty and Chitty test (Krebs, 1989) was used to test for equal catchability. MRR population analysis was carried out using the computer program JOLLY (Hines, 1988), using model A which takes into account variable deathrate and immigration.

3.3. Effective trap radius

Animals may enter traps from the surrounding area as well as from within the trapping grid. To obtain an estimate of population density from the population abundance data, it is necessary to calculate the effective trap radius. The method of Otis et al. (1978) provides a useful estimate and requires that a square trapping grid is set up with traps set the same distance apart. For the fox populations in Mahazat, effective trap radius was investigated on four occasions in summer–autumn 1997, with25 traps set for four consecutive nights,in a 5 5 square with1 km between traps.

3.4. Fox diet

Samples of faeces were collected from the first occasion each fox was captured in 10 trapping periods from September 1992 to January 1994, 4 periods in 1997, and were assumed to be representative of the prey consumed within the previous 12 h. 2985 faeces of V. ruppelli. sabea and 339 of V. vulpes arabica were analysed in ARTICLE IN PRESS

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1992–94 and 210 of V. ruppelli. sabea in 1997. In addition, 296 faeces of V. ruppelli. sabea cubs were collected from breeding dens in Spring 1993. Samples were sun-dried and then transferred to plastic bags and frozen until analysis. After de-frosting, each sample was dried and weighed to 0.01 g and prey items >0.5 mm were identified under a binocular microscope, using a reference collection. Dietary analysis was based on frequency of occurrence of prey types, an often used measure of diet (Dickman and Huang, 1988).

3.5. Radio-tracking

The aim of the radio-tracking study was to investigate the home range, movement and activity of adult V. ruppelli. sabea. 28 individuals were radio-tracked for at least 3 months in 1992–94 (14 male, 14 females) and 4 individuals (3 male, 1 female) in 1998. There were insufficient resources and time to investigate V. vulpes arabica and only 4 adults were tracked for 3 or more months in 1992–93. The study animals were trapped in the existing trap grids, fitted with a radio collar (Biotrack Ltd., Dorset, UK) and released in the early morning. The data from the first 3 days of tracking were not used, because these may have been influenced by the animals getting used to the radio collars. Radio fixes were obtained from a vehicle using a hand-held two- element antenna and a radio receiver (LA12, AVM Instruments Co., USA) and location recorded using a Global Positioning System. It was attempted to obtain radio fixes every 15 min withonly two or threeanimals being studied per night.To increase the accuracy of radio-fixes, foxes were approached carefully to reduce the transmitter–receiver distance. Activity data were obtained from changes in the pulse rate of the transmitter signals and by direct observation. Radio collars were retrieved by setting traps for each study within their home range at the end of the study period. The 95% minimum convex polygon was used to calculate the home ranges of the foxes, using the program CALHOME (Kie et al., 1994). Ideally radio tracking is continued until the number of fixes has accumulated so that an asymptote for home range size has been reached (Harris et al., 1990). Time constraints meant that this was not always possible, but there were at least 40 fixes (and usually over 60) per animal in this study for home range estimations.

3.6. Data analyses

Standard data analyses methods were used in this study. Chi-squared was always based on the frequency data (counts), but results have been given as percentages for clarity.

4. Results

During Phase 1 there was a total of 6240 and during Phase 2 a total of 3800 trap nights (2880 inside, 920 outside Mahazat). A mean of 6% of trap nights were forfeited because the trap was sprung with no animal inside or the bait was taken ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 51

Table 2 Total captures (including recaptures), number of different individuals and capture rate (individuals captured/trap night) of mammalian carnivores at Mahazat as-Sayd in Phase 1 (1992–94) and Phase 2 (1996–98) (6% of trap nights lost to trap failure)

Species Phase 1: inside Mahazat Phase 2: inside Mahazat Phase 2: outside Mahazat

Total Individuals Rate Total Individuals Rate Total Individuals Rate

V. vulpes arabica 113 82 0.014 111 81 0.030 5 3 0.003 V. ruppelli. sabea 1719 588 0.100 1029 287 0.106 46 22 0.025 Mellivora capensis 11 — 11 — 0 0 0 F. silvestris tristrami 3 3 0.001 5 5 0.002 2 2 0.002 F. margarita harrisoni 16 11 0.002 6 5 0.002 3 3 0.003 F. domesticus 4 2 0.001 0 0 0 4 4 0.005

Table 3 Effective trap radii (km) for foxes in Mahazat, based on 5 5 grids of traps set 1 km apart

V. ruppelli. sabea V. vulpes arabica

Summer 1997 1.43 a Autumn 1997a 0.95 2.26 Autumn 1997b 0.94 2.09 Autumn 1997c 0.76 0.98 Mean 1.02 1.78

a Insufficient captures/recaptures for calculation to be possible.

without the trap shutting. The total captures of carnivores (Table 2) clearly shows the greater capture of individuals of V. ruppelli. sabea than the other carnivores and also the lower captures rates of foxes outside of Mahazat. The capture rate of V. ruppelli. sabea was almost unchanged from Phase 1 to 2, but the rate for V. vulpes arabica was about double in Phase 2. All the sand cats (F. margarita harrisoni) and 82% of V. ruppelli. sabea caught outside of Mahazat were trapped in Area O3 (in the east), which had the most diverse vegetation and least human disturbance. The feral cats (F. domesticus) were caught in the vicinity of Bedouin camps outside of Mahazat and they were captured very occasionally inside Mahazat near to the research camps.

4.1. Effective trap radius

The mean effective trap radius for V. ruppelli. sabea was 1.02 km and for V. vulpes arabica 1.78 km (Table 3). Thus with the traps set 1 km apart in the 5 2 grids, the mean effective area trapped in Phase 2 was 17.5 and 31.8 km2 per grid for V. ruppelli. sabea and V. vulpes arabica respectively and 210.0 km2 (9.4% of land area) and 381.6 km2 (17.0%) within Mahazat. In Phase 1 the effective areas trapped were 69.9 and 99.3 km2 respectively. ARTICLE IN PRESS

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4.2. Sex ratio, juveniles and breeding

The sex ratio of new captures of adult V. ruppelli. sabea was significantly biased to males in both trapping Phases (Phase 1. 59:41% male:female; Phase 2 61:39%, chi- square po0.05 for both). For V. vulpes arabica the sex ratio of new captures of adults was balanced in Phase 1 (49:51% male:female) but significantly biased to females in Phase 2 (35:65% male:female, chi-square po0.05). Juvenile foxes of V. ruppelli. sabea (under 1 year old) made up 42%, 54% and 41% of new captures in 1992, 1993 and 1997 respectively and were most prevalent in summer and autumn eachyear (on average 65% of new captures in theseperiods). Juvenile V. vulpes arabica were more prevalent than adults, making up 75%, 80% and 67% of new captures in 1992, 1993 and 1997 respectively. Observations of the foxes indicated that mating took place in October–November and cubs were born from January to February. The juveniles tended to disperse from June to October, with the majority of longer movements being recorded in August–September. The timing of events for V. ruppelli. sabea was 2 to 4 weeks later than for V. vulpes arabica. In 1992 and 1993, detailed observations were made of 19 breeding females of V. ruppelli. sabea. The number of cubs per litter ranged from 2 to 6, with a mean of 3.3. The older females had a mean litter size of 3.7 cubs in contrast to a mean of 2.4 for one-year old females (t-test, po0.05).

4.3. Population density and survival

The mean density of V. ruppelli. sabea was 1.05 km2 in 1992–93 and 0.72 km2 in 1997. However, in 1992–93, the study area encompassed a much smaller area of Mahazat. Thus, allowing for the accuracy of the MRR method, the density of V. ruppelli. sabea was not significantly different from 1992–93 to 1997. The minimum number alive (MNA), a direct enumeration method of population estimation, can be viewed as the lower limit to the population abundance. In 1992–93 and 1997, the population density was highest in the summer and the peak was 1.9 to 1.5 times greater than the lowest point. Mean residence rates (MRR) and mean residences time (MRT) were calculated from recapture duration decay plots for all the recapture data following the methods of Cook et al. (1967). Losses to the marked population can be from mortality and from dispersal away from any of the trapping grids, which is why residence is the term used rather than survival. For V. ruppelli. sabea the annual MRR was 0.704 (70.4%), which gave a MRT of 8.4 months, with no significant difference between males and females. The oldest individual recaptured of V. ruppelli. sabea was a female 5.5 years old. The survival rates based on the Jolly–Seber calculations (Table 4) were for the 3 month period up to the date shown. For 1997, the rates were comparable to the MRR from the pooled data. The number of captures/recaptures of V. vulpes arabica was low in bothPhases and produced similar densities (Table 5). In addition, for V. vulpes arabica the annual MRR was muchlower at 0.203 (20.3%) (MRT 2.4 months)withdata for ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 53

Table 4 Population data for Vulpes ruppelli. sabea within Mahazat in 1992–93 and 1997, based on the Jolly–Seber (JS) method and minimum number alive (MNA)

Phase 1, 1992–93 Autumn Winter Spring Summer Autumn

JS, abundance 65 64 59 110 69 JS, SE abundance 10 11 9 14 12 MNA 48 46 36 80 52 JS survival rate 0.85 0.95 0.95 0.75 0.65 Mean population density (km2) 0.93 0.92 0.84 1.57 0.99 SE population density (km2) 0.14 0.16 0.13 0.20 0.17

Phase 2, 1997 All Mahazat Winter Spring Summer Autumn

JS, abundance 166 152 169 115 JS, SE abundance 14 12 14 12 MNA 127 134 135 92 JS, survival rate 0.71 0.76 0.85 0.65 Mean population density (km2) 0.79 0.73 0.81 0.55 SE population density (km2) 0.07 0.06 0.07 0.06

Standard errors are given when there were sufficient recaptures for the calculation. Goodness of fit test for all Jolly–Seber calculations indicated that the model was acceptable.

Table 5 Population data for Vulpes vulpes arabica within Mahazat in 1992–93 and 1997, based on the Jolly–Seber (JS) method (1997 only, insufficient recaptures in 1992–93) and minimum number alive (MNA)

Phase 1, 1992–93 Autumn Winter Spring Summer Autumn

MNA 7 5 20 6 5 Mean population density (km2) 0.07 0.05 0.20 0.06 0.05

Phase 2, 1997 All Mahazat Winter Spring Summer Autumn

JS, abundance 12 16 45 11 MNA 12 9 25 11 Mean population density (km2) 0.03 0.04 0.12 0.03

Standard errors and survival rates could not be calculated from the Jolly–Seber model with the available data.

males and females combined due to the low recapture rate. The oldest individual recaptured of V. vulpes arabica was a female 4.6 years old. The mean abundance of V. ruppelli. sabea was six to seven times greater than that of V. vulpes arabica (Tables 4 and 5) and, allowing for the differences in effective area trapped, the mean density of V. ruppelli. sabea was 12–13 times greater. The estimated peak and mean populations of V. ruppelli. sabea within the Mahazat Protected Area in 1997 were 1818 and 1616 respectively, and for V. vulpes arabica ARTICLE IN PRESS

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269 and 123. It is not possible to make this estimate for 1992–93 because the study area was much smaller. Based on capture rates in 1997, the populations of these fox species were about 5 and 10 times greater inside Mahazat than outside for V. ruppelli. sabea and V. vulpes arabica respectively (Table 2).

4.4. Fox diet

The analysis of remains in faeces revealed that the two fox species took a wide variety of food items, ranging from vertebrates, arthropods and plant matter (Table 6). Invertebrates (especially beetles) and small mammals were the most important food items, followed by vegetation (mainly seeds and fruit), withbird and reptile remains occurring only occasionally. The quantitative analysis showed these two fox species had broadly the same diet in Mahazat, with no significant differences (Mann– Whitney U-test) in 1992–94 (Table 7). Opportunism was observed when significant

Table 6 Food remains identified in the faeces of V. ruppelli. sabea and V. vulpes arabica in Mahazat

Category Taxa identified

Small mammals Rodentia (Gerbillus spp., Meriones spp.) Reptiles Lacertidae (e.g. Uromastyx spp.), Serpentes Birds Passerines (Laniidae, Timallidae, Alaudidae) Beetles (Coleoptera) Carabidae (Thermophilum spp.), Tenebrionidae (Mesotena, Pimelia, Blaps spp.), Histeridae (Saprinus spp.), Scarabidae Other invertebrates Isoptera, Hymenoptera (ants), Scorpiones, Solifugae, Orthoptera (Schistocera gregaria) Vegetation, seeds Acacia spp., Fagonia spp., Indigofera spp., Graminae, Leguminosae Others Sand, gravel, unidentifiable remains

All these taxa were identified in the faeces of both fox species.

Table 7 Dietary composition of V. ruppelli. sabea and V. vulpes arabica based on the analysis of faeces collected from 10 trapping periods from September 1992 to January 1994, and four trapping periods in 1997 for V. ruppelli. sabea only (% frequency is based on the number of faeces containing the food item per sample period; sd is standard deviation)

% Frequency V. r. sabea 1992–94 V. r. sabea 1997 V. v. arabica 1992–94

Mean sd Mean sd Mean sd

Small mammals 72.7 24.6 68.5 18.5 79.6 24.6 Reptiles 1.9 1.4 12.5 5.0 2.4 2.5 Birds 1.6 1.6 23.9 12.5 2.4 5.2 Beetles 32.9 25.1 71.6 19.5 38.3 26.1 Other invertebrates 90.7 7.6 91.5 12.6 85.2 14.4 Vegetation, seeds 36.7 10.9 73.5 16.7 36.3 14.5 Others 18.9 15.9 90.2 20.2 25.7 24.7 ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 55 amounts of the desert locust (Schistocera gregaria) occurred in the faeces in the summers of 1993 and 1997, which coincided with observed high populations of this insect at these times in Mahazat. There were significantly higher proportions of plant, and reptile (U-test, po0.05 for all three items) remains in faeces of V. ruppelli. sabea in 1997 compared to 1992–94. Withregard to small mammal prey, it was possible to identify to species level much of the remains and in 1992–94 there proved to be a significant difference in the utilisation of small mammals between V. ruppelli. sabea and V. vulpes arabica.The proportions of Meriones crassus, Gerbillus cheesmani and G. nanus were 12%, 47% and 41% for V. ruppelli. sabea, and 21%, 66%, and 13% for V. vulpes arabica (chi- squared=20.1, df=2, po0.05). The diet of V. ruppelli. sabea cubs was dominated, as withadults, by small mammals (59% frequency in faeces), invertebrates (38%) and notably by beetles (85%). Cubs were often observed feeding on beetles, which seemed to be a key part of their diet and probably helped them to develop their foraging skills.

4.5. Fox weights and length

There were no significant differences in the mean weights of adult foxes in the two Phases of study thus the data have been combined (Table 8). Female foxes were significantly lighter on average (t-test, po0.001 for bothspecies) thanmales, by 10.8% for V. ruppelli. sabea and 15.0% for V. vulpes arabica. Bothsexes of bothspecies were

Table 8 Weights (g) and body length (mm) of first captures of adult Vulpes ruppelli. sabea and Vulpes vulpes arabica within Mahazat

N Mean sd Minimum Maximum

Vulpes ruppelli. sabea Weight Males 306 1715 98 1260 2150 Females 233 1530 88 1270 1910 (t-test, po0.001)

Body length Males 41 472 18 425 510 Females 31 454 18 410 490

Vulpes vulpes arabica Weight Males 35 2846 189 2400 3250 Females 51 2418 175 2080 3000 (t-test, po0.001)

Body length Males 14 590 29 520 630 Females 14 559 18 535 585 ARTICLE IN PRESS

56 D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 about 10 to 15% heavier in the winter months (December–February) than the rest of the year (t-test, po0.05 for V. r. sabea, not significant for V. v. arabica). For 18 sub-adult V. ruppelli. sabea for which there were sequential recaptures, there was an increase in weight (on average) from 1190 g (sd=105) in summer to 1450 g (sd=115) in autumn of the year in which they were born. Body lengthmeasurement were collected for adult foxes in winter–spring 1993 and showed that females were smaller than males by 3.8% for V. ruppelli. sabea and 5.3% for V. vulpes arabica (t-test, po0.05 for bothspecies).

4.6. Home range and spatial organization

Seasonal home range sizes of foxes, based on individuals for which there were sufficient fixes, were larger for adult males than females of V. ruppelli. sabea by 27% in winter and 31% in summer (t-test, po0.05 for both), but there was no difference in the all year home ranges (Table 9). The larger size of the ‘all year’ home ranges was largely due to the different utilization of the area around the dens in summer and winter, and because eight foxes shifted their dens between seasons by distances of 2–5 km, moving their home range accordingly. The home ranges of pairs overlapped extensively, witha mean of 77% overlap based on female home ranges or 61% overlap based on male home ranges. Based on the limited radio-tracking study and direct observations, it appeared V. vulpes arabica lived a more nomadic life in Mahazat and only temporarily occupied particular home ranges. Therefore, definite boundaries of home ranges were more difficult to establishand neighbouring adults did not seem to occupy ranges that bordered on each other. An annual home range of 27.3 km2 was estimated for the single female V. vulpes arabica for which there were sufficient fixes for the necessary calculations. Foraging ranges of 4.5 (female), 6.1 (male) and 9.3 km2 (male) were estimated for three V. vulpes arabica for 3 monthperiods in 1992–93 before eachdispersed outside of thestudy area.

4.7. Activity, movement and dispersal

Data for V. ruppelli. sabea showed strictly crepuscular/nocturnal activity patterns, based on over 1700 independent fixes of radio-tracked foxes, which remained quite

Table 9 Home ranges (km2) of adult V. ruppelli. sabea within Mahazat based on radio-tracking, November–March and April–September, and for the whole year (for individuals tracked in both seasons)

Nov–MarchApril–Sept All year

Mean (sd, n) Mean (sd, n) Mean (sd, n)

Males 8.5 (2.2, 12) 7.7 (2.2, 12) 13.5 (5.4, 6) Females 6.7 (2.4, 10) 5.9 (2.2, 13) 13.1 (7.0, 7)

Home range based on 95% minimum convex polygons (MCP) (n is number of samples, sd is standard deviation). ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 57 constant throughout the year. The onset of activity was strongly linked to sunset, with the foxes emerging about 1 h after sunset. In contrast, the time when activity ceased was not directly linked to sunrise, so that the foxes had approximately the same lengthof activity period regardless of season, of about 11–12 h.Foxes were recorded as resting, typically 4–6 times, during the activity period, with rests lasting from 5 to 32 minutes (mean 14 min). Movements of V. ruppelli. sabea within home ranges were considerable during the activity period witha maximum of 9 km recorded by radio-tracking data and the mean distance travelled was 4.8 km. Longer distance movements of 7 sub-adult males were monitored in 1993. These foxes moved well away from their natal areas, to a mean distance of 22 km (range 5–28 km, and the latter fox’s route was 48 km in length). The one sub-adult female that dispersed away from her natal area, moved 7 km and set up a new home range which she maintained for at least the next 9 months. In 1997, 5 male and 5 female sub-adults had moved between trapping grids in Mahazat, based on the MRR study (mean distance 25 km, maximum 68 km). Less data were available for V. vulpes arabica but large dispersal movements were recorded for sub-adults. In 1993 four males dispersed distances of between 20 and 36 km and two females bothmoved 20 km. In 1997, two females moved 15 km between trapping grids.

5. Discussion

V. ruppelli. sabea (Ruppell’s. fox) proved to be the most abundant small carnivore both inside and outside of the fenced Protected Area of Mahazat as-Sayd. The population was about four times greater inside Mahazat, based on capture rate, probably due to the absence of persecution by humans and the improving habitat conditions, exemplified by greater plant diversity. V. vulpes arabica (Arabian red fox) had a considerably lower density than V. ruppelli. sabea within Mahazat, and lower still outside the fence. The other small carnivore species had low abundance compared to the foxes, but appeared to be have self-sustaining populations within Mahazat. Although population estimates of V. ruppelli. sabea fluctuated over the course of the study, with peaks occurring in summer and autumn, this is probably due to the emergence of juveniles from dens which is reflected in the higher proportion (65%) of juveniles/sub-adults caught at this time. Although the trapping area and protocol were not identical in the two phases of research, there was no strong evidence for any change in the population density of V. ruppelli. sabea. The abundance of V. vulpes arabica might have increased two-fold based on capture rate, but the direct enumeration method (MNA) produced very similar estimates of population density in the two phases. In a long-term 15 year study of Vulpes macrotis mutica (San Joaquin kit fox) in a semi-arid region of California the population density varied widely over a 15 year study from 0.21 to 1.68 km2 (Cypher et al., 2000). The values for V. ruppelli. sabea of 0.72–1.05 km2 were well within this range for a similar small fox species in a broadly similar habitat. ARTICLE IN PRESS

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There have been very few published data on survival rates for foxes in arid areas. The estimated annual survival/residence rate for V. ruppelli. sabea was 70% (based on mean residence rate method) and was 39% based on the Jolly–Seber method (note the values in Table 4 were for 3 month periods, the mean is 0.791 for the 9 periods, 0.7914=0.392). The annual survivorship of Vulpes macrotis mutica in California was 44% (range 20–81%) (Cypher et al., 2000). For a Vulpes vulpes (Red fox) population in NorthAmerica, annual survival rates were just under 20% ( Storm et al., 1976) and similar estimates were made for Urocyon cinereoargenteus (Gray fox) (Wood, 1959). These values were similar to the estimates made in Mahazat for V. vulpes arabica, but the data were less reliable due to the lower number of captures and greater movement of these foxes, which took them out of the trapped areas. Prior to this study, the only information on reproduction by V. ruppelli. sabea was based on very few cases (e.g. one or two litters only in: Roberts, 1977; Lindsay and Macdonald, 1986; Linn, 1990;). The maximum litter size of six was twice as large as reported before and the mean of 3.3 is higher than the previously reported typical litter size of two. Adult V. vulpes arabica were significantly larger and heavier than V. ruppelli. sabea, but the overall range of items in their diets were similar. Faecal analyses have been widely used as a non-intrusive method for determining the diet of carnivores (Huey, 1969; Dickman and Huang, 1988) and although some under and over-estimation of the prey is likely due to different digestibility, this could not be corrected for in the present study. Small mammals were certainly an important component of the foxes’ diet, with a frequency (69–80%) very similar to that reported by Lindsay and Macdonald (1986) for V. ruppelli. sabea in Oman (71%). An interesting difference in the small mammals taken by the two fox species was noted in Mahazat, with V. vulpes arabica preying proportionately more on the larger species Meriones crassus and V. ruppelli. sabea preying more on the smallest species Gerbillus nanus. Birds were evidently a very muchless important part of thediet, a result also found by Lindsay and Macdonald (1986). Whilst still a generalist, invertebrates were clearly important for V. ruppelli. sabea and a wide variety were consumed, thus the species appears to be more insectivorous than other arid zone fox species (V. vulpes arabica, this study; V. macrotis mutica, White et al., 1996). Huey (1969) noted that smaller species of canids are not strictly carnivorous. Fruits and vegetables are often added to the diet when available. This was evidently the case for foxes in Mahazat. The significantly higher proportion of plant remains in faeces of V. ruppelli. sabea in 1997 compared to 1992– 94 was likely to be linked to the noted progressive increase in plant species richness and cover in Mahazat since the area was fenced (Collenette, 1997). The more diverse vegetation was likely to support higher populations of birds and reptiles, which may also explain the higher frequency of these items in the faeces of V. ruppelli. sabea in 1997. The results of this study confirmed the conclusions of Lindsay and Macdonald (1986) that adult V. ruppelli. sabea live as territorial pairs throughout the year. These pairs were the basic social units of the population, as the male and female occupied largely congruent home ranges. The home range sizes were between 6 and 9 km2 in ARTICLE IN PRESS

D.M. Lenain et al. / Journal of Arid Environments 57 (2004) 45–60 59 the winter or summer seasons and the foxes were evidently active throughout the night in their home range foraging for food. These home ranges are similar to the mean of 11 km2 reported V. macrotis mutica (Cypher et al., 2000). For carnivores have to forage over a larger range than granivores or herbivores because of the sparser distribution of their food (Davis and Houston, 1984). The largely constant activity period of V. ruppelli. sabea throughout the year has also been noted for Vulpes cana (Blandford’s fox) by Geffen et al. (1992a) who estimated that the foraging activity of V. cana was very costly, requiring about 8 times more energy expenditure than at rest. Longer dispersal movements of V. ruppelli. sabea were noted. Almost all offspring (sub-adults) dispersed from the natal range at 7–10 months of age and it would appear that they moved until they found a vacant area or formed a pair with an establish adult. Foxes could move several tens of kilometers. Lenain and Warrington (2001) showed that translocated V. ruppelli. sabea could travel long distances to return to their original area (up to 100 km) and one adult male travelled 71 km in 11 days. Based on a mean home range of 7.2 km2 (mean of the 4 values in Table 9) each witha pair of V. ruppelli. sabea foxes rearing 3 juveniles, the estimated population size in the Mahazat Protected Area would be 1558. This value is remarkably similar to the 1997 population estimate of 1616 (and maximum of 1818) based on the Jolly– Seber method and the effective trap radii. Thus the two approaches to estimating the population size provide good agreement on the fox population size and show that V. ruppelli. sabea is the most abundant small carnivore species in this arid zone area.

Acknowledgements

We are grateful for the support of His Royal Highness Prince Saud Al Faisal, Managing Director of the NCWCD, Dr. Abdulaziz Abuzinada, Secretary General of the NCWCD, and Jacques Renaud, General Manager of the National Wildlife Research Center (NWRC). Special thanks go to Phillip Seddon and Olivier Combreau for their considerable help with this project.

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