HABITAT ECOLOGY OF TWO SYMPATRIC SPECIES OF JACKALS IN ZIMBABWE
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1 Journal of Mammalogy, 83(2): , 2002 HABITAT ECOLOGY OF TWO SYMPATRIC SPECIES OF JACKALS IN ZIMBABWE A. J. LOVERIDGE AND D. W. MACDONALD* Wildlife Conservation Research Unit, Department of Zoology, South Parks Road, Oxford OX1 3PS, United Kingdom We radiotracked 22 jackals, 11 Canis mesomelas and 11 Canis adustus, in Hwange, Zimbabwe, to test the hypotheses that habitat use would differ and that the larger C. adustus would displace the smaller C. mesomelas. C. mesomelas preferentially used grassland. C. adustus used woodland and scrub. Habitat use by C. adustus differed from allopatric populations in which this species uses grassland, the likely favored habitat for jackals. C. mesomelas was shown to aggressively displace C. adustus from grassland. Aggressive displacement of a larger species by a smaller species is an unusual and probably unique behavior in carnivores. Key words: Zimbabwe aggression, Canis adustus, Canis mesomelas, habitat partitioning, jackal, sympatry, Two species of jackals occur in southern Africa. The side-striped jackal (Canis adustus) is found throughout central Africa as far south as Zimbabwe and northern South Africa. The distribution of the black-backed jackal (Canis mesomelas) extends throughout South Africa, Namibia and Botswana and into Zimbabwe, occurring as far north as the Zambesi escarpment, but the species is not present in the Zambesi valley or north of the Zambesi River. The 2 species occur in sympatry over most of south and central Zimbabwe (Fig. 1) and northern Botswana (Smithers 1983). This study was undertaken within the region of sympatry for the 2 species of jackals in northwestern Zimbabwe. In general, sympatric canids differ in weight by a factor of 2 or more (Wayne et al. 1989); however, southern African jackals are more similar in size (Smithers 1983; Van Valkenburgh 1991; Van Valkenburg and Wayne 1994). In southern Africa C. mesomelas are generally smaller than C. adustus (Smithers 1983). In studies of sympatric canids the clear trend is for larger * Correspondent: david.macdonald@zoology.ox.ac.uk species to kill or displace smaller ones, resulting in habitat partitioning. For example, in Europe and North America, red foxes (Vulpes vulpes) displace arctic foxes (Alopex lagopus Hersteinsson and Macdonald 1992; Rudzinski et al. 1982), coyotes (Canis latrans) exclude red foxes (Harrison et al. 1989; Sargeant and Allen 1989; Voigt and Earle 1983), and wolves (Canis lupus) may kill or supplant coyotes (Carbyn 1982; Thurber et al. 1992). In northern Africa, a similar situation occurs between wolves and golden jackals (Canis aureus Dayan et al. 1992), and golden jackals may kill red foxes in Israel (Macdonald 1987). Likewise, in Australia, dingos (Canis familiaris dingo) kill red foxes (Marsack and Campbell 1990), and in South America the culpeo (Dusicyon culpaeus) uses interspecific aggression to displace the smaller chilla (Dusicyon griseus) to habitats with poorer resources (Jiménez et al. 1996; Johnson and Franklin 1994a, 1994b). The 3 species of jackals in East Africa also show habitat segregation (Fuller et al. 1989; Kingdon 1977; Wyman 1967), although the mechanism 599
2 600 JOURNAL OF MAMMALOGY Vol. 83, No. 2 FIG. 1. Map of Zimbabwe showing the geographic ranges of Canis mesomelas (horizontal shading) and C. adustus (vertical shading) after Smithers (1983). The area where the 2 species of jackal are sympatric is shown with crosshatching. The study area is shown, shaded black, on the border of Hwange National park (H.N.P.). through which this is achieved is unknown. Rautenbach and Nel (1978) suggest that because of similar habitat preferences, size, and activity patterns, C. adustus and C. mesomelas probably compete in the Transvaal of South Africa. Johnson et al. (1996) suggest that the mechanism responsible for what is often perceived as differing habitat preference may be exclusion of a subordinate species from habitats with the best resources. The subordinate species survives in areas that are suboptimal to the dominant species, either because of lower energetic requirements or because of specialist adaptations of the displaced species. In this study we tested the hypothesis that C. mesomelas and C. adustus segregate habitat in a similar way to other sympatric canids, with the larger displacing the smaller into suboptimal areas where the smaller species body size or other adaptations allow it to survive. MATERIALS AND METHODS Study area. The 2,785-ha study site was on a private wildlife estate adjacent to Hwange National Park (18 45 S, E), Zimbabwe (Loveridge and Macdonald 2000). Habitat composition of the study site was measured from aerial photographs taken in Areas of habitats were estimated by hand using a grid overlay and ground-truthed during fieldwork in the study area. The vegetation of the area was predominantly teak woodland (Baikiaea plurijuga; 2,076 ha, 75% of the study area). Grassland made up 18% of the study area (493 ha), and Terminalia sericea ecotone scrub (144 ha, 5% of the study area) provided the interface between teak woodland and grassland. Small stands of camel-thorn acacia (Acacia erioloba; 47 ha, 1.7% of the study area) were found adjacent to the grassland. Humans were found to have settled in a small proportion ( 1%) of the area, and 5 waterholes were present. Capture, radiotelemetry, and behavioral observations. Eleven C. adustus and 11 C. mesomelas were trapped and collared. Jackals were trapped using padded foothold traps (Victor softcatch No. 2, Woodstream Inc., Lititz, Pennsylvania). Trapped jackals were weighed and measured, sex was determined, and radiocollars (200 g, Biotrack Ltd., Waring, Dorset, United Kingdom; Frequency MHz) were fitted. A colored and numbered 3 by 1-cm eartag (Rototag, Dalton supplies Ltd., Nettlebed, United Kingdom) was attached to the right ear. Movement sensors were incorporated into the radiocollars to determine activity of collared jackals at night. Mass of radiocollars was below the recommended collar-to-body-mass ratio of 3% (Cypher 1997). Radio transmitters were detectable at approximately 2 km and had an effective field life of 18 months. Radiocollared jackals were tracked from a vehicle, with an M57 receiver (Mariner Radar, Lowestoft, Suffolk, United Kingdom) and a roof-mounted omni-directional antenna (Telonics Inc., Mesa, Arizona) for initial location. For each fix, rapid ( 1 min) 2-station triangulations were taken, at least 50 m apart, with a 4-element yagi antenna (Loveridge and Macdonald 2000). Fixes for rapidly moving jackals were not taken. Jackals were mostly active at night, and peak nocturnal activity periods for both species occurred after sunset and before sunrise (Loveridge 1999). Radiotracking was undertaken between July 1995 and September 1996 and was sequentially rotated among instrumented animals so that each
3 May 2002 LOVERIDGE AND MACDONALD INTERSPECIFIC COMPETITION IN JACKALS 601 was followed for 2 nights before repeating the sequence. Where feasible (i.e., adjacent or overlapping home ranges) up to 2 animals were simultaneously followed in 1 tracking period. For each jackal, fixes were obtained every 10 min over 8 h, from dusk to midnight or midnight to dawn, on alternate nights. Tracking accuracy was determined during trials where an assistant hid a transmitter in an undisclosed position, enabling comparison between actual and estimated positions. Hidden transmitters were relocated at distances comparable to those used when tracking jackals. Accuracy was to within an average of 10 m of the actual position (n 10; SD 10.4). Bearings were transferred to 1:25,000 aerial survey maps (Zimbabwe, Kamativi 1314, 1316, 1318, 1320) and the jackal s position recorded along with details of activity and habitat. Day-time position and activity were assessed approximately once a week, between 1000 and 1500 h. A total of 191 fixes for 7 C. mesomelas and 146 fixes for 10 C. adustus were obtained between November 1995 and September Interspecific interactions (n 23) were recorded between January and August 1996 at distances from 5 to 50 m from the observer during routine fieldwork. In order to solicit interactions between jackals, on 5 occasions recordings of either rabbit (Sylrilagus) distress calls or sounds of a hyena (Crocuta crocuta) kill were played to attract jackals for observations. A speaker was set up 30 m from a vehicle, in an area where both species of jackals were known to be present, and the sound played for 1 min followed by 10 min of observation. Jackals very rapidly became habituated to these sounds, so they were only used once in each jackal territory. Data analysis. Weights of trapped jackals were compared between sexes and species in MINITAB GLM (general linear model) using log-transformed weights (Ryan et al. 1985). In order to determine an appropriate sample of fixes to accurately describe home range size, cumulative home range size was plotted against fix number (cf. Doncaster 1990; Doncaster and Macdonald 1991; White and Garrot 1990). An asymptote was approached at fixes. Using a sample 150 of fixes, calculated home ranges also closely approximated hand-drawn estimates based on behavioral observations and chance sightings. Radiotelemetry data were analyzed using a nonparametric home-range analysis program (WILDTRAK Todd 1992). Habitat use was analyzed at 2 levels (2nd and 3rd order selection Johnson 1980). First, minimum convex polygons (Mohr 1947) were drawn on a habitat map. The resulting aggregate outline of all ranges was defined as the study area. Habitat-use data were combined for each species and compared with habitat availability within the entire study area (as defined previously). The 2nd level of analysis addressed habitat use and availability within individual home ranges. The restricted polygon method (Wolton 1985) was used to calculate individual home ranges. Restricted polygons are defined as polygons in which no side exceeds the mean distance of all fixes from the arithmetic mean center. This method, unlike minimum convex polygons, excludes large areas of unused ground and is not sensitive to extreme outlying fixes (Mills 1990). Habitat availability within restricted polygons was calculated and compared with actual use by the individual jackals. Individuals for which there were insufficient radio fixes ( 150) or which were not tracked for a sufficient period ( 3 months) were eliminated from the sample. Mated pairs were not used in analysis of habitat use because habitat choice may not be independent. Comparison of nocturnal habitat use with habitat availability at both the study area (2nd order habitat selection) and home range (3rd order habitat selection) level followed the compositional method of Aebischer et al. (1993). This method reduces serial correlation (Swihart and Slade 1985) by using the animal rather than the radiolocation as the sample unit, although De Solla et al. (1999) showed that autocorrelation of radiofixes does not affect the precision or accuracy of home-range estimates if animals are tracked over a biologically meaningful time period. Proportions of active to inactive fixes and choice of diurnal resting habitats were compared between species in MINITAB GLM (Ryan et al. 1985) using arcsine-transformed proportions. RESULTS Jackals trapped in the study area differed significantly in size between sex (F 9.1, d.f. 1, 21, P 0.007) and species (F 98.6, d.f. 1, 21, P 0.001) (C. adustus males: 10.1 kg, n 4, SD 0.6, range ; females: 9.6 kg, n 6, SD 0.4, range ; C. mesomelas males: 7.6
4 602 JOURNAL OF MAMMALOGY Vol. 83, No. 2 FIG. 2. Illustration of Canis mesomelas and C. adustus home ranges (restricted polygons) in relation to the distribution of grassland habitat (gray outline) during June August Human habitation is shown with a circle. C. mesomelas home ranges were closely associated with grassland; C. adustus ranges were found in the surrounding woodland, often close to human settlement. kg, n 6, SD 0.8, range ; females: 6.6 kg, n 8, SD 0.58, range ). Order of entry into the sequential general linear model did not affect the conclusions. Each jackal was radiotracked for a mean of 7.3 months (SD 4.8, range 1 15) during which time a mean of 16.4 tracking sessions (SD 12.6, range 1 48) were undertaken per individual, yielding a mean of 488 fixes (SD 356, range 12 1,200) per jackal. Three jackals (1 C. adustus, 2 C. mesomelas) were excluded from the analysis because they had been tracked for 3 months or had fewer than 150 radiofixes, either because of mortality or because of capture late in the study. Mean areas of home ranges based on nocturnal fixes were ha for C. mesomelas and ha for C. adustus (Loveridge and Macdonald 2000). Nocturnal habitat use by individuals within the entire study area (2nd order selection) shows that selection of habitat was significantly nonrandom for both species (C. mesomelas: , d.f. 5, P 0.001; C. adustus: 2 33, d.f. 5, P 0.001). Furthermore, within their home ranges (3rd order selection), jackals used habitats nonrandomly in relation to their availability (C. mesomelas: , d.f. 5, n 9, P 0.004; C. adustus: , d.f. 5, n 10, P 0.042). Although individual variations occurred, C. mesomelas used grassland more than its availability might suggest. Woodland (especially Baikiaea) was used considerably less than expected (Figs. 2 and 3). Canis adustus preferred Terminalia ecotone and avoided grassland. Baikiaea woodland was used either less than or in approximate proportion to its availability. Acacia and waterholes made up only small proportions of the study area, and there were no obvious trends in the use of these habitats by either species. However, the home ranges of all 6 known mated pairs of C. adustus were centered on human habitation (4 near safari camps and 2 in the vicinity of a hotel). Both species of jackal used human habitation to a greater extent than expected based on availability, which is probably indicative of scavenging behavior. The relative values for habitat availability in relation to habitat use by C. adustus and C. mesomelas (Fig. 3) indicate that although Baikiaea woodland was the most predominant habitat, it is also the most underutilized by both species. Grassland was used to a far greater extent than expected by C. mesomelas and slightly less than expected by C. adustus. Habitat use by C. adustus conformed more closely to availability, although there are clear preferences for Terminalia scrub and human habitation. Canis mesomelas was more active during the day (27%, n 52) than C. adustus (11%, n 16; F 4.6, d.f. 1, 16, P 0.049). The proportion of resting fixes in grassland was significantly different (P ) between the 2 species, with C. mesomelas found resting in this habitat most
5 May 2002 LOVERIDGE AND MACDONALD INTERSPECIFIC COMPETITION IN JACKALS 603 FIG. 3. Mean divergence of actual from expected habitat use based on habitat availability within home ranges, by Canis mesomelas and C. adustus in the Dete vlei study site. A value of zero represents expected habitat use, and positive and negative values represent relative use of particular habitats to a greater or lesser extent than expected. Error bars show standard deviation. Habitat types are abbreviated as follows: GL grassland, TS Terminalia sericea scrub, BW Baikiaea woodland, AW Acacia woodland, WH Waterhole, HH Human habitation. often (Fig. 4). Resting sites in Baikiaea woodland also differed significantly (P ) between species, with C. adustus more likely to be inactive in this habitat. In 21 of all 23 observed interspecific interactions, either C. mesomelas chased C. adustus from the vicinity (14 occasions) or C. adustus retreated or avoided the presence FIG. 4. Percentage of inactive diurnal fixes in various habitats for Canis mesomelas and C. adustus. Inactive diurnal fixes comprised 73% of total fixes for C. mesomelas and 89% of fixes for C. adustus. Total fixes for C. mesomelas equals 139, whereas that of C. adustus equals 130. of C. mesomelas with no chasing (7 occasions). In 8 of these cases a food resource or potential food resource (i.e., recorded sound) was available. On only 2 occasions were both species present with no interaction. In 1 of these cases the 2 groups of animals were separated by 50 m. On 10 occasions C. mesomelas chased C. adustus when no food resource was available to defend. In these cases, pursuits of between 15 and 50 m occurred, and all followed a similar pattern. In 3 of the 22 interactions, C. adustus retreated from C. mesomelas, without being chased, C. mesomelas showing no signs of having noticed the other animals. In other cases (n 8), a food resource or potential food resource (recording of prey distress calls) was involved in the interaction. On 4 occasions, C. adustus did not attempt to approach in the presence of C. mesomelas but instead stayed in the vicinity, using Terminalia scrub as cover. On 2 of these occasions, C. adustus fed later, and on the other 2 occasions they never gained access to the food resource, possibly because C. mesomelas remained in the area or because the resource was consumed by other scavengers. Both species responded to sound recordings on 2 occasions. In both
6 604 JOURNAL OF MAMMALOGY Vol. 83, No. 2 cases, C. mesomelas aggressively displaced C. adustus. DISCUSSION Habitat use by jackals varies considerably between different areas, based not only on habitat availability but also on the presence or absence of other species of jackals. Some clear trends in habitat use emerge for each of the species in areas of sympatry. C. aureus uses dry open grassland (Kingdon 1977; Lamprecht 1978; Wyman 1967). C. mesomelas uses open woodland when sympatric with C. aureus (Fuller et al. 1989), but in the absence of this species in southern Africa it uses open grassland in addition to open woodland and scrub (Smithers 1983). C. adustus tends to use densely vegetated habitats whenever it is sympatric with another species of jackal (Fuller et al. 1989; Kingdon 1977; Pienaar 1969; Smithers 1983; this study). This habitat specificity is not found when these species are allopatric. Where C. mesomelas is allopatric in southern Africa it shows wide habitat tolerance, with habitat use ranging from desert in Namibia to montane regions of South Africa (Nel 1984; Rowe-Rowe 1982; Smithers 1971, 1983; Stuart 1976, 1981). Similarly, when allopatric, C. adustus occupies a wide range of habitats and appears especially to use grassland. In areas where C. adustus is allopatric in Senegal, Uganda (Ruwenzori National Park), Zambia, and northern Zimbabwe, this species is frequently found in grassland and avoids woodland (Ansell 1960; Atkinson 1997; Kingdon 1977; C. Sillero-Zubiri, pers. comm.). It is clear that in the absence of competitors C. adustus and C. mesomelas both choose to use grassland and open woodland over other habitats. We showed that in an area where C. mesomelas and C. adustus are sympatric, C. mesomelas occupy grassland resting sites and use grassland habitat to a greater extent than does C. adustus. C. mesomelas did not use woodland habitats and, as appears to be the case in other areas, showed an aversion to thick vegetation (Pienaar 1969; Stuart 1981; Smithers 1983). C. adustus used Baikiaea woodland and Terminalia ecotone but entered grassland far less often than would be expected from the availability of this habitat. Diamond (1975) hypothesized that, in the absence of interspecific competitors, a species will expand its range into all favorable habitats (competitive release). In the case of the 2 southern African species of jackals, it is clear that in the absence of C. mesomelas (e.g., northern Zimbabwe Atkinson 1997), C. adustus will use a range of habitats and preferentially use grassland, the most favorable habitat. However, when the 2 southern African species are sympatric, the range of habitats used by C. adustus is narrowed, in response to the presence of the smaller but more aggressive species. The habitat partitioning observed in this study appears to be mediated by aggressive exclusion of C. adustus from grassland by C. mesomelas. Because jackals are coursing predators adapted to open terrain (Ewer 1973, Johnson et al. 1996), grassland appears to be a favorable habitat with access to more resources and resting places. Open grassland allows easy movement, and open resting sites may facilitate vigilance for potential predators (e.g., leopard, Panthera pardus Turnbull-Kemp 1967). In addition, Atkinson (1997) found that guinea savannah grassland in central Zimbabwe (cf. Coe and Skinner 1993) is richer in food resources, such as small mammals and fruit, than is woodland and therefore tends to be frequented more often than expected by C. adustus. In this study, grassland also provided habitat suitable for springhares (Pedetes capensis), a prey item favored by jackals (Ferguson 1980; Loveridge 1999; Nel 1984). Relationships between sympatric species of canids are often hostile, and in general larger species dominate (Carbyn 1982; Major and Sherburne 1987; Rudzinski et al. 1982). However, despite their smaller size and contrary to expectation, C. mesomelas appeared to be dominant to C. adustus. In
7 May 2002 LOVERIDGE AND MACDONALD INTERSPECIFIC COMPETITION IN JACKALS 605 interspecific encounters C. mesomelas almost always aggressively displaced C. adustus, with C. adustus avoiding direct confrontation with C. mesomelas. Kingdon (1997) suggests that C. mesomelas are generally more aggressive than other jackal species. There is evidence that they may also displace C. aureus (Kingdon 1977). C. mesomelas is also more likely to risk feeding among lions (Panthera leo) and spotted hyenas (Crocuta crocuta) at carcasses than are other species of jackals (Estes 1967, 1991; Kingdon 1977; Mills 1990; Wyman 1967). Aggression by a smaller sister species leading to interspecific domination has also been shown in salamanders (Anthony et al. 1997) as has domination by smaller over larger conspecifics in Drosophila (Zamudio et al. 1995) and nymphalid butterflies (Hernandez and Benson 1998). In such cases, aggression or superior vigor allows a smaller species or individual access to resources that might otherwise be monopolized by a larger potential competitor. Maynard-Smith and Parker (1976) called this intrinsic domination behavior in asymmetric contests resource holding potential. Clearly, because of its size advantage, C. adustus might be expected to be more successful in interspecific contests. However, contrary to our hypothesis, C. mesomelas appears to have resource holding potential in its more aggressive behavior, which apparently counteracts any disadvantage derived from smaller size. ACKNOWLEDGMENTS We thank A. Elliot and L. Reynolds for allowing this study to take place on the Hwange estate. A. J. L. was funded by a Beit Trust Fellowship. P. Johnson assisted in the analysis of habitat use. The authors benefited from the extensive suggestions of H. Kruuk and C. Perrins and 2 anonymous journal referees. J. Church, A. Killmer, A. Radford, L. Bonesi, G. Thomas, and P. Lindsay helped with radiotracking. LITERATURE CITED AEBISCHER, N. J., P. A. ROBERTSON, AND R. E. KEN- WARD Compositional analysis of habitat use from animal radio-tracking data. Ecology 74: ANSELL, W. F. H Mammals of northern Rhodesia. The Government Printer. Lusaka, Zambia. ANTHONY, C. D., J. A. WICKNICK, AND R. G. JAEGER Social interactions in two sympatric salamanders: effectiveness of a highly aggressive strategy. Behaviour 134: ATKINSON, R. P. D The ecology of the sidestriped jackal (Canis adustus Sundevall), a vector of rabies in Zimbabwe. D.Phil. dissertation, University of Oxford, Oxford, United Kingdom. CARBYN, L. W Coyote population fluctuations and spatial distribution in relation to wolf territories in Riding Mountain National Park, Manitoba. Canadian Field-Naturalist 96: COE, M. J., AND J. D. SKINNER Connections, disjunctions and endemism in the eastern and southern African mammal faunas. Transactions of the Royal Society of South Africa 48: CYPHER, B. L Effects of radio-collars on San Joaquin kit foxes. Journal of Wildlife Management 61: DAYAN, T., D. SIMBERLOFF, E. TCHERNOV, AND Y. YOM- TOV Canine carnassials: character displacement in the wolves, jackals and foxes of Israel. Biological Journal of the Linnean Society 45: DE SOLLA, S. R., R. BONDURIANSKY, AND R. J. BROOKS Eliminating autocorrelation reduces biological relevance of home range estimates. Journal of Animal Ecology 68: DIAMOND, J. M Assembly of species communities. Pp in Ecology and evolution of communities (M. L. Cody and J. M. Diamond, eds.). Harvard University Press, Cambridge, Massachusetts. DONCASTER, C. P Non-parametric estimates of interaction from radio-tracking data. Journal of Theoretical Biology 143: DONCASTER, C.P.,AND D. W. MACDONALD Drifting territoriality in the red fox, Vulpes vulpes. Journal of Animal Ecology 60: ESTES, R. D Predators and scavengers. Natural History 76:20 29, ESTES, R. D The behavior guide to African mammals, including hoofed mammals, carnivores and primates. University of California Press, Berkeley. EWER, R. F The carnivores. Cornell University Press, Ithaca, New York. FERGUSON, J. W. H Die ekologie van die rooijakkals, Canis mesomelas Schreber 1778 met spesiale verwysing na bewegings en sociale organisaise. M.Sc. thesis, University of Pretoria, Pretoria, South Africa. FULLER, T. K., A. R. BIKNEVICIUS, P. W. KAT, B. VAN VALKENBURGH, AND R. K. WAYNE The ecology of three sympatric jackal species in the Rift Valley of Kenya. African Journal of Ecology 27: HARRISON, D. J., J. A. BISSONETTE, AND J. A. SHER- BURNE Spatial relationships between coyotes and red foxes in eastern Maine. Journal of Wildlife Management 53: HERNANDEZ, M.I.M.,AND W. W. BENSON Small
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