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Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2004? 2004 834 527538 Original Article DIETS OF SYMPATRIC CANIDS AND FELIDS O. B. KOK and J. A. J. NEL Biological Journal of the Linnean Society, 2004, 83, 527–538. With 2 figures Convergence and divergence in prey of sympatric canids and felids: opportunism or phylogenetic constraint? O. B. KOK1 and J. A. J. NEL2* 1 Department of Zoology and Entomology, University of the Free State, PO Box 339, Bloemfontein 9300, South Africa 2 Department of Zoology, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa Received 14 April 2003; accepted for publication 2 April 2004 Since the canids and felids diverged in the mid-Eocene or earlier, each family has developed a suite of morphological and behavioural adaptations for obtaining and consuming prey. We here distinguish between prey taxa captured and eaten as a result of these phylogenetic adaptations, and those because they are fortuitously encountered, and argue that such supplementary prey, often opportunistically caught, create a buffer between sympatric, and potentially competitive, canids and felids and thus enhance coexistence. We base our analysis on dietary data derived from the stomach contents of four sympatric canid and felid species in the Free State Province, South Africa (canids: Cape fox Vulpes chama and black-backed jackal Canis mesomelas; felids: African wild cat Felis silvestris lybica and caracal Caracal caracal), and from results of studies on these species elsewhere in southern Africa. The two canid species preyed heavily on invertebrates, and thus opportunistically, while the felids (especially the caracal) concentrated on mammals, prey they are phylogenetically adapted to capture. Only three species of mammalian prey are shared by the four species. The ratio of opportunistically-to-phylogenetically mediated prey taxa used (the O/P ratio) differ between the species, with the black-backed jackal having the most opportunistically caught taxa in its diet, and the caracal the least. As predicted, a comparison of this data with those from dietary studies of the same species carried out elsewhere indicates that the number of opportunistically obtained prey taxa varies more than those resulting from phylogenetic adaptations. The largest canid had the widest food spectrum (35 prey taxa) while the smallest felid had the most restricted one (11 prey taxa). We argue that using the O/P distinction allows a better understanding of changes in food niche breadth of particular species, especially in xeric areas, and gives a better indication of possible exploitative competition for food by sympatric carnivores than when regarding all prey taxa as actively pursued. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538. ADDITIONAL KEYWORDS: coexistence – competition – diet – food niche – phylogeny. INTRODUCTION The diet of a carnivore reflects both the availability of its potential prey items, as well as a suite of morphological, behavioural and physiological adaptations that allow the individual to locate, capture, ingest and digest a variety of prey taxa. While food availability varies both spatially and temporally, evolutionary adaptations are more rigid, but do allow some degree of plasticity to the predator in obtaining and processing prey not commonly captured. Carnivore guilds commonly consist of a number of species differing in size, taxonomic affinities, and mor*Corresponding author. E-mail: [email protected] phological and behavioural characteristics that help adapt them for capturing and ingesting a diverse prey spectrum (e.g. Rosenzweig, 1966; Van Valkenburgh, 1985, 1988; Dayan & Simberloff, 1996). Coexistence of such sympatric carnivore species can be explained by both evolutionary divergence (e.g. Van Valkenburgh, 1985, 1989) as well as ecological interactions and mechanisms (MacArthur & Levins, 1967; Schoener, 1974, 1982). Evolutionary divergence can manifest itself in, for example, dentition and skull morphology, and in locomotor adaptations (Van Valkenburgh, 1985, 1989), while ecological mechanisms include the partitioning of the trophic, spatial and temporal axes of the niche (Levins, 1968) amongst others. In this regard differential selection of different prey species © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 527 528 O. B. KOK and J. A. J. NEL (Karanth & Sunquist, 2000), different prey sizes (Gittleman, 1985; Karanth & Sunquist, 2000), different habitats for foraging (Palomares et al., 1996), different activity patterns (Fedriani, Palomares & Delibes, 1999; Karanth & Sunquist, 2000), and differential use of space (Creel & Creel, 1996; Palomares et al., 1996; Durant, 1998) have been proposed. During their independent evolutionary history since the mid-Eocene or earlier, some general family-specific strategies and adaptations for capturing and consuming prey have evolved in the canids and felids (Ewer, 1973; Van Valkenburgh, 1985), so that today they differ in both morphology and behaviour. Canids are typically long-legged coursers, have retained the original carnivore dentition of 42 permanent teeth and postcarnassial molars, affording them the ability to evolve into a diversity of dental and dietary types (Van Valkenburgh, 1991), and are more opportunistic or omnivorous (Kleiman & Eisenberg, 1973). Both the carnassials and postcarnassials afford some crushing surface (Van Valkenburgh, 1989); retention of the postcarnassial molars also allows the individual greater flexibility in its diet, and perhaps the ability to survive changes in prey availability (Van Valkenburgh, 1991). Felids, on the other hand, typically remain concealed and ambush and stalk their prey, using only a short rush or charge (Elliot, Cowan & Holling, 1977; Kruuk, 1986) followed by a quick killing bite (Eisenberg, 1981; Skinner & Smithers, 1990). They kill prey as large or larger than themselves. Small felids also often pounce on small prey, e.g. rodents (Kruuk, 1986). Felids have a short rostrum and have a much reduced dentition of only 30 permanent teeth. There is only one upper molar, but the molars are the most specialized for a carnivorous life, with no crushing surfaces on either the carnassials or postcarnassials (Eisenberg, 1981; Van Valkenburgh, 1989). Felids can therefore be expected to be specialized in their diet as they are consistently hypercarnivores, but although highly specialized have been a very successful morphotype over evolutionary time (Van Valkenburgh, 1991). Canids and felids therefore differ both in their anatomical adaptations for prey location, capture and killing (Ewer, 1973; Van Valkenburgh, 1985; Biknevicius & Van Valkenburgh, 1996), and in prey-catching behaviour (e.g. Ewer, 1968). For most felid species food can also be assigned to significantly fewer categories than for canids (Kruuk, 1986). This would primarily result from the highly specialized felid dentition. The degree of specialization in a particular species can be demonstrated by comparing its diet in different areas, using Kendal’s coefficient of concordance (Siegel, 1956). This measures the degree of agreement (concordance) between different sets of rank orderings of the same set of parameters, e.g. the diet of a species in different regions. Previous studies show that felids all have high coefficients of concordance, i.e. they specialize on a restricted food spectrum, while canids have lower coefficients (Kruuk, 1986), eat a wider range of food categories, and are usually termed ‘generalists’ or ‘opportunists’; the two terms are often used interchangeably, and seldom defined. Although the diet of a felid species can closely correspond in different areas, suggesting that it is either highly selective of habitats or highly specialized in hunting techniques, or both (Kruuk, 1986), between-area differences can and do occur. In southern Africa this can be ascribed to an unstable prey base such as major fluctuations in rodent numbers, or to differences in the availability of prey species or food categories, as has been found in the caracal (Smithers, 1971; Avenant & Nel, 1998). Although primarily carnivorous, smaller felids such as the black-footed cat Felis nigripes Burchell and the African wild cat Felis silvestris lybica Forster (we here follow Bronner et al. (2003) in recognizing F. s. lybica as a subspecies) also consume a variety of invertebrate taxa (Avenant, 1993; Sliwa, 1994; Kok, 1996; this study). The two canids used in this study are the Cape fox Vulpes chama (A. Smith) and the black-backed jackal Canis mesomelas Schreber, and the two felids are the African wild cat and the caracal Caracal caracal (Schreber). In southern Africa they are sympatric and often syntopic over most of their geographical range (Mills & Hes, 1997). They often share habitats and are all mostly nocturnal, with black-backed jackal and, to a lesser extent the caracal, also being partially diurnal in some areas (Avenant & Nel, 1998; Loveridge & Macdonald, 2003). All are terrestrial, with the African wild cat also being partially arboreal, and all are carnivorous with a range of prey items being shared by two or more species. Examination of the diets of these species in our study area suggested that the capture and ingestion of some prey items result from their evolutionary adaptations in morphology, especially dentition, and behaviour as outlined above. Other prey items again include very small prey taxa such as invertebrates, which the carnivores are not specifically adapted to capture; the inclusion of these items in many cases probably resulted from fortuitous encounters. Such prey are much more variable both intra- and interspecifically, as well as geographically. This suggests that the diet of a particular carnivore should be regarded as consisting of two components: one resulting from evolutionary adaptations (basic prey), and the other resulting from chance encounters (supplementary prey). This helps to explain the coexistence of some sympatric carnivores, because the supplementary component can act as a dietary buffer between species that are competing for the same basic prey over and above differences due to evolutionary © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 DIETS OF SYMPATRIC CANIDS AND FELIDS adaptations. We also predict that the supplementary prey component will tend to vary more between different areas, for a particular predator species or between species. Low levels of basic prey availability should therefore result in a higher proportion of supplementary prey, even in specialized hunters such as felids. While optimization of foraging and feeding plays a major role in the immediate decision of which prey to select, evolutionary constraints limit the possibility of either locating, or of capturing and consuming a particular prey item. We argue that a more accurate picture of the diet, and therefore of the food niche, of each predator species, and consequently of the overlap or separation in a carnivore guild, can be obtained by separating these two prey categories. Differences in the ratio of opportunistically-to-phylogenetically mediated prey captured (the O/P ratio) could therefore be indicative of either changes in the basic prey base for a particular species, or of changes in the degree of exploitative competition between sympatric carnivore species. Despite the disappearance of large carnivores from our study area, it is doubtful if those here examined currently exhibit any competitive release as far as their prey is concerned. Only the black-backed jackal that commonly scavenges could be influenced by the lack of ungulate carcasses due to predation by large predators. The four predator species investigated here are still widespread in southern Africa. Results from this analysis could therefore also be used to compare the diets of the same species in different parts of their range, where one or more of the other species may be absent. This will provide insight into the effect of decreased competition for food on diet. The hypothesis that we test is that the supplementary prey category, mostly acquired due to fortuitous encounters, will vary much more between different localities for the same predator species, than the basic prey category, i.e. those prey captured and consumed because the predator is morphologically and behaviourally adapted to do so. In addition canids, due to their less specialized dentition and coursing behaviour, would have more supplementary prey taxa included in their diet than felids, resulting in a lower Kendal’s coefficient of concordance. Furthermore we suggest that supplementary prey acts as a buffer between carnivore species occurring in sympatry, and could lessen exploitative competition so as to enhance coexistence. MATERIAL AND METHODS To test the above assumptions, we here use two data sets to determine differences and overlap in the diets of four sympatric canids and felids. We compare (1) the stomach contents of the four carnivores from the Free 529 State Province of South Africa, which derives from our own field research; (2) published results of various relevant studies in southern Africa. Our own data and those of Smithers (1971) are, however, the only results that allow comparison of the four species in sympatry, albeit on different spatial scales. As analyses by different authors vary in resolution, these published results on prey identity cannot always be directly compared, at least not at the species level. However, comparison at higher taxonomic levels, or using arbitrary mass categories, is possible. Stomach contents of 293 black-backed jackals, 76 Cape foxes, 57 caracals and 19 African wild cats were collected in the Free State in South Africa during all seasons over a period of 8 years (July 1984–July 1992) during predator control operations by Oranjejag, a now defunct predator control organization, and preserved in 70% ethyl alcohol or 10% formaldehyde. Stomach contents were sorted macroscopically in the laboratory and dried at 75 ∞C for 48 h in an Inc-O-Mat drying oven. Food items were identified to the lowest taxonomic level possible, using a stereoscopic microscope and a reference collection of potential prey. For all taxa, the frequency of occurrence was calculated as the proportion of stomachs containing the taxa, expressed as a percentage of the total number of stomachs analysed. For a comparison of the diet of the same predators elsewhere in southern Africa, and for calculating Kendal’s coefficient of variation (Siegel, 1956) published data were used. These were Grafton (1965); Bothma (1966a, 1966b, 1971a, 1971b); Smithers (1971); Lynch (1975); Stuart (1976, 1981); Smithers & Wilson (1979); Bester (1982); Rowe-Rowe (1983); Bothma, Nel & Macdonald, (1984); Moolman (1986); Palmer & Fairall (1988) and Avenant & Nel (1992). The prey categories used were Arachnida, Insecta, Reptilia, Aves, Artiodactyla, Carnivora, Hyracoidea, Lagomorpha and Rodentia (all four species), and in addition, for the Cape fox also the Myriapoda and Macroscelidea. For an interspecific comparison of the number of food categories, the above categories as well as carrion and vegetable (fruits) were used. Most studies report on stomach content analyses, with a few based on faecal analyses. As the degree of resolution in the various analyses differs, direct comparison of prey species and other aspects are not always possible. For each carnivore species all vertebrate prey was allocated to the basic category, unless a higher taxon was captured at < 5% frequency of occurrence (e.g. Osteichthyes). In xeric parts of South Africa small mammal population size fluctuates widely over a number of years and < 5% frequency of occurrence in the stomachs probably reflects low population numbers of a particular prey species rather than the car- © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 530 O. B. KOK and J. A. J. NEL nivore not being phylogenetically adapted to capture it. All invertebrate prey were regarded as the supplementary category, unless personal observations on foraging predators indicated otherwise (see below). The weights of non-vertebrate prey were obtained from Kok (unpubl. data) and those of mammalian prey from Lynch (1983) or Skinner & Smithers (1990). RESULTS The ratio of males to females in the sample of specimens for each carnivore species from the Free State did not deviate from parity. Likewise, no gender differences in the dietary composition of the different predator species could be demonstrated (MANOVA, P = 0.05). Dietary data for males and females within each species were therefore combined. Clear differences in the number of prey taxa consumed by the canids and felids studied emerged, with more prey taxa represented in the diets of the two canid species (Tables 1 and 2). These differences are significant between (P = 0.01) but not within (P = 0.05) families. In both families the smaller species had a more restricted diet, but both species of canid fed on a broader prey spectrum than the largest felid (Table 1, Fig. 1). Canids also included more invertebrates in their diet, both as regards the number of taxa and in comparison to the caracal, also as the percentage of total occurrence. For the Cape fox the respective values were 10 and 45.5%, respectively; for the blackbacked jackal 14 and 40.0%; for the African wild cat 5 and 45.5%; and for the caracal 3 and 17.65%. Both canids captured a more representative sample of taxonomic categories and weight class categories as food (Figs 1, 2). In both families the smaller species took more invertebrates than the larger ones (notably in the case of the African wild cat) but only slightly fewer mammals (Fig. 1). The caracal captured a much Table 1. Composition of prey in the diet of 76 Cape foxes ( Vulpes chama), 293 black-backed jackals (Canis mesomelas), 19 African wild cats (Felis silvestris lybica) and 57 caracals (Caracal caracal), in the Free State Province, South Africa. Class totals in bold V. chama (2.8 kg) C. mesomelas (8.5 kg) F. s. lybica (4.5 kg) C. caracal (16 kg) Prey taxon A B C A B C A B C A B C Invertebrate Arachnida (total) Acarina Araneae Scorpionida Solifugae Crustacea Diplopoda Insecta (total) Blattodea Coleoptera Dermaptera Diptera Hymenoptera Isoptera Lepidoptera Mecoptera Orthoptera Plecoptera (Unidentified) 1.3 – – 1.1 0.1 – – 72.7 – 24.6 0.9 29.8 0.2 1.4 2.9 – 12.8 0.1 – 0.1 – – 0.1 < 0.1 – – 6.4 – 2.2 0.1 2.6 < 0.1 0.1 0.3 – 1.1 < 0.1 – 4 – – 1 3 – – 37 – 17 3 8 1 4 13 – 16 1 – 3.9 – 0.3 0.6 3.0 0.4 0.5 224.6 0.1 121.7 0.8 13.9 14.3 24.3 4.4 0.3 34.6 – 10.2 0.1 – < 0.1 < 0.1 < 0.1 < 0.1 < 0.1 2.5 < 0.1 1.4 < 0.1 0.2 0.2 0.3 0.1 < 0.1 0.4 – 0.1 4 – 4 1 1 <1 1 31 <1 21 1 4 4 7 3 <1 7 – 2 0.7 – – – 0.7 – – 6.2 – 4.8 – – 0.1 0.4 – – 0.9 – – 0.2 – – – 0.2 – – 2.1 – 1.7 – – <0.1 0.1 – – 0.3 – – 5 – – – 5 – – 26 – 16 – – 5 5 – – 5 – – 0.1 0.1 – – – – – 8.1 – 8.0 – – – 0.1 – – – – – < 0.1 < 0.1 – – – – – 0.2 – 0.2 – – – < 0.1 – – – – – 2 2 – – – – – 5 – 1.6 – 0.2 – 3 – – – – – – – 16 86 3 3 2 <1 1 10 89 2 – – 1.5 91.8 0.2 1.5 0.1 < 0.1 < 0.1 2.8 93.2 3.2 – – 17.2 1037.3 2.7 129.5 5.0 2.1 2.9 246.1 8332.5 287.0 – 284.1 115.8 – 97.6 39.8 – 90 26 17.8 5628.6 21.5 0.3 99.5 0.4 5 97 2 Vertebrate Osteichthyes Reptilia (total) Chelonia Squamata Aves (total) Mammalia (total) 1. Lepus capensis 4 – – – 2 – – – – – © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 DIETS OF SYMPATRIC CANIDS AND FELIDS 531 Table 1. Continued V. chama (2.8 kg) C. mesomelas (8.5 kg) F. s. lybica (4.5 kg) C. caracal (16 kg) Prey taxon A B C A B C A B C A B C 2. Hystrix africaeaustralis Pedetes capensis Xerus inauris Aethomys namaquensis Rhabdomys pumilio Saccostomus campestris Tatera spp. Desmodillus auricularis (Unidentified) 3. Elephantulus myurus (Unidentified) 4. Cynictis penicillata Ictonyx striatus Suricata suricatta Otocyon megalotis Caracal caracal 5. Orycteropus afer 6. Procavia capensis 7. Antidorcas marsupialis Raphicerus campestris Redunca fulvorufula Sylvicapra grimmia Capra hircus Ovis aries (Unidentified) Mammals unidentified to order – – 5.9 150.1 18.0 – 97.3 – 135.8 2.0 2.0 4.0 – – – – – 0.7 – 90.0 – – – 187.2 6.0 335.6 – – 0.5 13.3 1.6 – 8.6 – 12.0 0.2 0.2 0.4 – – – – – 0.1 – 8.0 – – – 16.6 0.5 29.7 – – 4 11 3 – 7 – 18 1 1 1 – – – – – 1 – 3 – – – 5 3 33 92.3 436.1 76.5 440.0 25.0 – – – 382.2 – – 2.5 1.3 234.6 – 66.2 108.5 145.2 912.7 1476.5 – 1016.2 191.1 1786.9 310.7 341.0 1.0 4.9 0.9 4.9 0.3 – – – 4.3 – – < 0.1 < 0.1 2.6 – 0.7 1.2 1.6 10.2 16.5 – 11.4 2.1 20.0 3.5 3.8 1 6 2 3 1 – – – 15 – – <1 <1 2 – 1 <1 2 2 12 – 9 2 19 2 9 – – – 18.6 21.5 – 57.2 9.1 26.5 – – – – – – – – 29.5 – – – – – – – 5.9 – – – 6.4 7.4 – 19.7 3.1 9.1 – – – – – – – – 10.1 – – – – – – – 2.0 – – – 11 5 – 16 5 21 – – – – – – – – 5 – – – – – – – 11 – – 33.0 89.8 – 61.0 – – 74.8 – – 97.5 – – 105.0 – – 857.0 652.0 6.4 11.9 1054.6 12.3 1864.5 191.3 496.0 – – 0.6 1.6 – 1.1 – – 1.3 – – 1.7 – – 1.9 – – 15.2 11.5 0.1 0.2 18.7 0.2 33.0 3.4 8.8 – – 4 5 – 4 – – 11 – – 4 – – 2 – – 7 7 2 2 16 2 26 2 11 A, dry mass (g); B, dry mass per cent of total dry mass; C, frequency of occurrence (%) of taxon. 1- 7: Orders Lagomorpha, Rodentia, Macroscelidea, Carnivora, Tubulidentata, Hyracoidea, Artiodactyla. higher percentage of mammalian taxa than the other species and was therefore the most carnivorous, concentrating on mammal prey, while the black-backed jackal was the most omnivorous. The African wild cat had the most restricted diet, especially as far as the number (but not percentage) of mammalian prey was concerned. When prey are assigned to different weight classes it is clear that the canids prey more equitably on different-sized prey than the two felids (Fig. 2). Where the African wild cat captured a preponderance of smaller prey, the black-backed jackal but especially the caracal favoured large prey, with the latter species capturing a high percentage of prey heavier than itself. Clearly, as the size of both canid and felid species increases, so does the representation of prey larger than the mean body weight of the predator in its diet (see also Carbone et al., 1999). There were also differences in the number and identity of prey that were unique to each species. The larger species in each family had more unique prey species than the smaller one, with the black-backed jackal having the most. Many taxa, mostly mammals, were shared by the four species (Table 3), but only three prey species were common to all the carnivores. Comparisons of the mean percentage occurrence of the different prey categories from different areas (Table 4) show that the two canid species consume a much higher percentage of invertebrates than the two felids, and in particular insects. While the Cape fox nearly has equal representation of invertebrates and rodents in its diet, the African wild cat also consumes invertebrates, but clearly concentrates on rodents. The caracal takes nearly equal percentages of artiodactyls and rodents with the artiodactyls all heavier than itself, while the black-backed jackal has the most diverse diet. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 532 O. B. KOK and J. A. J. NEL Table 2. Number of prey taxa in the diet of four sympatric canid and felid species in the Free State Province, South Africa. Figures in parentheses indicate percentage occurrence: a single set refer to the total number of prey taxa for the species; in the case of a double set the first (preslash) refer to the total number of prey taxa, and the second (postslash) to the particular taxonomic category Predator Prey V. chama C. mesomelas F. s. lybica C. caracal Total no. of prey taxa in dieta Invertebrate prey taxa with < 5% freq. occurr. Vertebrate prey taxa (n.m)b with < 5% freq. occur. Mammal prey taxa with < 5% freq. occur. Invertebrate taxa of 1–5 g Invertebrate taxa of 6–10 g Vertebrate (n.m) taxa < 50 g > 50 g Mammal taxa of < 50 g 51–150 g 151–1000 g 1001–2500 g 2501–5000 g 5001–10 000 g 10 001–15 000 g 15 001–25 000 g 25 001–40 000 g > 40 000 g 22 10 6 2 1 10 7 7 3 5 8 2 2 2 1 1 1 1 – – – 35 14 11 4 3 17 13 10 4 3 18 3 – 4 1 2 1 1 1 1 3 11 5 0 0 0 6 0 3 2 2 4 3 1 – 1 1 – – – – – 17 3 3 1 0 13 8 3 – 3 14 2 – 2 1 2 1 – 1 2 2 a b (45.5) (26.1/60) (8.6) (4.3/50) (45.5) (30.4/70) (30.4) (13.0) (21.7) (34.8) (8.6/20) (8.6/20) (8.6/20) (4.3/10) (4.3/10) (4.3/10) (4.3/10) (40.0) (31.4/78.6) (11.4) (8.6/75) (48.6) (37.1/76.5) (28.6) (11.4) (8.6) (51.4) (8.6/17.7) (11.4/23.5) (2.9/5.9) (5.9/11.8) (2.9/5.9) (2.9/5.9) (2.9/5.9) (2.9/5.9) (8.7/17.7) (45.5) (54.5) (27.3) (18.2) (18.2) (36.4) (27.3/50) (9.1/16.7) (9.1/16.7) (9.1/16.7) (17.6) (17.6/100) (5.9) (76.5) (47.1/61.5) (15.0) (15.0) (70.0) (11.8/15.4) (11.8/15.4) (5.9/7.7) (11.8/15.4) (5.9/7.7) (5.9/7.7) (11.8/15.4) (11.8/15.4) Represents lowest taxonomic categories identified, and includes, Class, Order or Species (see Table 1). n.m, non-mammal. 100 Vulpes chama Canis mesomelas Felis s. lybica Caracal caracal 90 80 Percentage occurrence 70 60 50 40 30 20 10 0 Insects Arachnids Reptiles Birds Mammals Prey category Figure 1. Percentage occurrence of the major prey categories in the diet of four sympatric canid and felid species in the Free State Province, South Africa. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 DIETS OF SYMPATRIC CANIDS AND FELIDS 533 60 Vulpes chama Canis mesomelas Felis s. lybica Caracal caracal Percentage occurrence 50 40 30 20 10 0 < 5g 6–50 g 51–150 g 151–1000 g 1001–5000 g > 5000 g Mass class Figure 2. Percentage occurrence of the weight classes of prey, expressed as a percentage of the total percentage of all classes, in the diet of four sympatric canid and felid species in the Free State Province, South Africa. Table 3. Prey taxa shared by sympatric canid and felid species in the Free State Province, South Africa Vulpes chama Invertebrates Vertebrates (n.m)a Vertebrates (mammal) Canis mesomelas Invertebrates Vertebrates (n.m)a Vertebrates (mammal) Felis s. lybica Invertebrates Vertebrates (n.m)a Vertebrates (mammal) a Canis mesomelas Felis s. lybica Caracal caracal 2 7 2 5 8 2 classes 5 orders none 3 orders 5 species 1 2 1 5 7 2 classes 4 orders none 3 orders 4 species 1 class 2 orders 1 class 5 orders 10 species – – – – – – 1 class 2 orders none 3 orders 3 species classes orders classes orders species – – – class orders order orders species n.m, non-mammal. When use of prey categories, as compared to prey taxa, is compared, the Cape fox included 8.2 (of 11) in its diet, the black-backed jackal 9.7, the African wild cat 6.1, and the caracal 7.5. This again indicates that the two felids have a more restricted diet. PREY USE IN DIFFERENT AREAS Between-species comparisons for most areas were impossible as in most cases only one species was studied. Exceptions were the Free State, where two previ- © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 534 O. B. KOK and J. A. J. NEL Table 4. Mean percentage occurrence of different prey categories in the diet of sympatric canid and felid species in southern Africa, as derived from present data and published results. For a list of authors consulted, see Material and Methods Predator Prey category V. chama C. mesomelas F. s. lybica Invertebrates (total) Arachnida Insecta Vertebrates (total) Osteichthyes Amphibia Reptilia Aves Mammalia Artiodactyla Carnivora Hyracoidea Lagomorpha Rodentia 54.1 7.4 46.2 ? 0 < 0.5 8.7 14.6 44.3 6.6 38.3 ? 0.63 < 0.1 4.3 13.9 32.6 9.1 23.4 ? 0 1.1 4.6 13.1 5.9 2.9 3.0 ? 0 0 1.9 9.9 8.9 < 1.0 < 1.0 6.6 55.6 25.0 1.2 1.2 7.6 34.2 3.0 < 1.0 2.6 8.3 71.7 35.2 3.8 15.0 6.6 32.0 ous studies have been conducted, and Botswana. For the rest, between-area comparison for a particular species only could be attempted. THE CAPE FOX VULPES CHAMA In all studies arachnids had a low (< 10%), and insects a fairly high (24–60%) percentage of occurrence, except for Botswana, with a 35 and 96% occurrence, respectively. The same applies to reptiles, where the percentage occurrence varied from 3 to 12%, but was 30% in Botswana. Birds appeared consistently (7–26% occurrence) in the diet, as did lagomorphs and rodents. The use of insectivores (elephant shrews) was more sporadic. Disregarding livestock, predation on artiodactyls was nearly nonexistent. The appearance of individual insect orders in the diet varied, much more so than in the case of mammals, for example. However, the degree of occurrence of particular rodent species depended on the area, with the largest number of species being recorded in the diet in Botswana. Kendal’s coefficient of concordance was 0.72 (N = 9), indicating a fairly high degree of dietary specialization over its range. for the montane grasslands of the Drakensberg mountains, where several species had a high or unique representation. While insects and arachnids as food categories were usually well-represented, the occurrence and contribution by the different orders tended to vary greatly. Kendal’s coefficient of concordance was 0.65 (N = 9), indicating a lower degree of dietary specialization than in the Cape fox. THE AFRICAN BLACK-BACKED JACKAL CANIS MESOMELAS Several studies combined arachnids and insects into a single prey group, making comparisons difficult. However, insects, birds, artiodactyls and rodents always featured prominently in the diet. Rodent occurrence tended to show site-specific differences, especially so WILD CAT FELIS SILVESTRIS LYBICA African wild cats tended to predate consistently on arachnids and also insects. Birds were common vertebrate prey, as were rodents, while in some areas lagomorphs were also well represented in the diet. Ignoring small livestock, artiodactyls were virtually absent from the diet. Considering the large number of rodent species represented by all studies, this prey category is the most comprehensive of all. Kendal’s coefficient of concordance was 0.46 (N = 7), the lowest of the four species considered here. This indicates a fairly low level of dietary specialization in southern Africa. THE THE C. caracal CARACAL CARACAL CARACAL Fish and amphibians were absent and invertebrates and reptiles poorly represented in diets from different areas. A fair number of birds were taken while mammals, especially artiodactyls, hyraxes and rodents (and in two cases lagomorphs) featured prominently in the diet. The caracal was the only predator that took © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 DIETS OF SYMPATRIC CANIDS AND FELIDS prey heavier than itself throughout its range. Kendal’s coefficient of concordance was 0.55 (N = 8), indicating a medium degree of dietary specialization. CONVERGENCE AND DIVERGENCE IN DIETS Comparison of these results (Tables 1, 3, Fig. 1) with those of other studies (Table 4 and the references cited in Material and Methods) shows that convergence and divergence in diets occur both within, as well as between, the two families. To some extent this is a factor of the different-sized species being compared as in both families the smaller species has a more restricted diet in terms of the number of prey taxa captured than the larger (Table 1). Based on the percentage occurrence of prey, the smaller species also eats smallersized prey more often (Fig. 2). Both canids fed more frequently on invertebrates, and also more on nonmammal vertebrates, than the two felids. Conversely, felids fed more frequently on mammals (Fig. 1), and more often on larger prey relative to body weight (Fig. 2). Apart from size, the study area or habitat type or even the time of study could influence the results. For example, in our study no birds were recorded in the diet of the African wild cat, although previous studies in the Free State (Bester, 1982; Kok, 1996) did so. Some studies elsewhere also report amphibians, hyraxes and hares in the diet of this species. Convergence in prey between the two families therefore results primarily from the mammalian taxa shared, especially rodents, while divergence is highlighted by differences in the frequency of use of invertebrates, and non-mammal vertebrates, excepting birds. PREY CAPTURE: OPPORTUNISM VS. PHYLOGENY Based on prey taxa and percentage occurrence in the diet (Table 2), the number of opportunistically caught prey (all invertebrates and non-mammal vertebrates occurring at a frequency (£ 5%) could be determined. Comparing these with the number of prey resulting from phylogenetic adaptations gave an O/P ratio of 0.69/1 for the Cape fox, 0.67/1 for the black-backed jackal, 0.83/1 for the African wild cat and 0.21/1 for the caracal. These differences result from the larger number, or proportion, of invertebrate taxa in the diet of the canids and the African wild cat. Clearly the two canid species (especially the black-backed jackal) rely more heavily on fortuitously acquired prey than the two felid species. Invertebrates are, however, not always fortuitously acquired: black-backed jackals actively search for and eat harvester termites Hodotermes mossambicus (Hagen) (Ferguson, 1980; J. A. J. Nel, pers. observ.) as well as orthopterans and coleopterans (J. A. J. Nel, pers. observ.). However, the general distinction that is made here between prey 535 that are captured opportunistically, and those that are captured due to evolutionary adaptations, should hold true. DISCUSSION The stomach samples analysed for this study mainly came from areas where small livestock (sheep and goats) were available. Therefore to some extent our data are biased towards the inclusion of these two types of prey. However, African wild cats have never yet been recorded as preying on these two prey (Skinner & Smithers, 1990), while Cape foxes can only kill sheep less than 3 months old, otherwise they can only be used as carrion (Bester, 1982). The black-backed jackal and caracal can prey heavily on these livestock, which to some extent probably replaced wild ungulates lost due to widespread farming practices. However, where dietary composition in areas with and without small stock were compared, few differences were evident apart from the addition of livestock as prey for the caracal (Stuart, 1982; Moolman, 1986; Avenant, 1993). Elsewhere, the caracal always included a wide spectrum of mammals in its diet (Grobler, 1981; Palmer & Fairall, 1988). All studies point to caracals preying predominantly on mammals, with the prey range probably reflecting the availability of prey taxa. Even with a mass < 21.5 kg (but being closer to this transition point of Carbone et al. (1999)) the caracal is unique amongst the species compared here in feeding mostly on prey ~45% of its mass. In addition, there is a positive correlation between caracal use of habitat and prey density (Avenant & Nel, 1998). The same applies to the black-backed jackal. All the published studies (e.g. Bothma, 1966a, 1971a, 1971b; Smithers, 1971; Ferguson, 1980; Rowe-Rowe, 1983) indicate a catholic diet for the jackal, with relative occurrence of prey taxa differing widely between locations, probably as a response to availability. Domestic livestock clearly forms an addition to their normal diet and not a substitute for other items. Although having a more restricted diet than blackbacked jackal (Bothma, 1966a, 1966b; Skinner & Smithers, 1990; this study) Cape foxes similarly use lambs ~3 months old as an additional, and not a substitute, dietary item. Seasonal differences in use, related to lambing, are clearly apparent here (Bester, 1982). It should be kept in mind that as a carnivore matures and increases in mass its diet changes, and such changes have been documented for growing Cape fox pups in the Kalahari (Bester, 1982). For example, Diplopoda are only eaten by young foxes, never by adults. However, such data are few or nonexistent, depending on the species, and could not be used in the present comparison. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 536 O. B. KOK and J. A. J. NEL Data from our own study, and those from previous studies in the Free State and elsewhere in southern Africa support the contention of Kruuk (1986) that felids include fewer food categories in their diets than canids, especially if the size of predator is considered. In general, it also supports the suggestion by Van Valkenburgh (1989) that felids are highly specialized for capturing mammalian prey. However, this must be qualified by noting that the African wild cat captures nearly equal numbers of invertebrate and vertebrate prey taxa, albeit that the caracal concentrates heavily on mammals that are usually as heavy as or heavier than itself. The two canid species captured a wider range of taxa, a trend that is especially evident in the prey of the black-backed jackal, which in our study took more mammal species than the caracal. A more realistic appraisal of the diet of a species can be obtained by comparing results from studies undertaken in different localities, even accepting the difficulties that arise due to different prey categories being used. In southern Africa, our data and those of others indicate that the diets of the two canid species differ less, and have a higher Kendal’s coefficient of concordance, between sites than do the diets of the two felids species, which have a lower coefficient of concordance. These results therefore do not support the suggestion by Kruuk, (1986) that felid diets in different areas are more similar (suggesting a high degree of selection of habitats, or very specialized hunting techniques, or both) than those of canids. A probable explanation for this discrepancy is that our data derive from studies in mostly arid-to-semiarid habitats within southern Africa, where fluctuating and unpredictable rainfall events influence primary production in the first place, and through it available biomass in the ascending trophic levels. This means that the more opportunistic species, in this case the canids, would always find prey such as insects or rodents, no matter where they occur, and that they merely switch between whichever particular species is present. In the case of the phylogenetically more specialized felids, the nonavailability of a particular prey taxon could force them to be less selective in southern Africa, which would account for the lower coefficients of concordance recorded here. In more temperate habitats, however, food in a particular category would probably always be available, which would account for the higher degree of specialization being reflected in higher Kendal’s coefficients of concordance. For example, the European wild cat Felis s. silvestris has a coefficient of 0.67 (Kruuk, 1986) compared with the ecologically fairly similar Africa wild cat Felis s. lybica that has a coefficient of 0.46 (these results). As predicted, the fortuitous component of the diet varies more between different areas than that of the evolutionarily mediated one. This reduces the Kendal’s coefficient, which in effect means that canids are more opportunistic than felids. It can also be argued that searching techniques per se have an influence on the capture rate of supplementary prey. Coursers such as canids would flush many more insects or other invertebrates than felids, which stalk and tend not to be distracted from their selected prey. Because this opportunistic element depends heavily on the invertebrates consumed, this allows the creation of a buffer between the two families as far as prey sharing is concerned. However, the effect of the size of the predator is always present, with smaller carnivores feeding more heavily on invertebrate prey (Carbone et al., 1999). The effect of this buffer will increase as vertebrate, and especially bird and mammal prey, decreases. As prey availability decreases, predators become less selective and their food spectrum broadens. In southern Africa, and especially the xeric parts, rodent numbers tend to fluctuate widely. Therefore at low levels of abundance of these prey, canids can and do switch to a higher invertebrate component, but even felids can do so (Palmer & Fairall, 1988). This flexibility of canids is also demonstrated by comparing the geographical distribution of the four species here compared. In the hyperarid parts of southern Africa, such as the Namib Desert, Cape foxes and black-backed jackals can exist, but not caracal and African wild cats (Coetzee, 1969). Where the four species are sympatric, as in our study area and many other parts of southern Africa, slight differences in habitat use, activity (only the jackal and to a lesser extent the caracal are also diurnal) and few shared mammal prey species would lessen possible competition and mediate coexistence. We have suggested above that the food niche (Hutchinson, 1957) of a predator can be better understood if the dichotomy used here is taken into account. Because food niche breadth is affected by the number of taxa included in the diet as well as the equitability of their occurrence, it is obvious that a factor that heavily influences the number of taxa, as well as changes in frequency occurrence (dependence on invertebrates and scarce vertebrates), in the diet plays a major role in determining food niche breadth. To combine all prey in a single category obscures the reasons for dietary plasticity. From the above it will be evident that changes in the O/P ratio of predators in a given locality should be expected, and that these are caused by changes in the availability of specific prey taxa. A decrease in the availability of prey captured because of phylogenetic adaptations would tend to increase the reliance of the predator on opportunistically caught prey, and to increase the O/P ratio, while an increase in prey such as rodents would have the opposite effect, because selection for such a favoured prey would now be possible. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 527–538 DIETS OF SYMPATRIC CANIDS AND FELIDS In conclusion, we suggest that by assigning prey taxa to two categories, i.e. those that are caught opportunistically and those that are hunted because of the evolutionary adaptations of the predator, a better idea of the prey of carnivores can be obtained. Furthermore, this dichotomy is especially useful when comparing sympatric and potentially competing predator species. In addition to slight differences in habitat use and activity rhythms and sharing only a few mammal prey taxa, such a dichotomy in the prey spectrum would help explain coexistence of sympatric carnivores that seemingly overlap in their broad prey spectrum. Furthermore, it would also be more meaningful, and biologically correct, to contrast specialist with generalist when referring to the range of prey used by predators. The term opportunist or opportunism should be therefore confined to those instances where prey are indeed opportunistically captured after being fortuitously encountered, i.e. where the search phase of the prey acquisition sequence is absent. ACKNOWLEDGEMENTS We are indebted to J. du P. Bothma, M. J. Somers and two anonymous referees for many suggestions which helped to improve this paper. However, we remain responsible for all errors or omissions. REFERENCES Avenant NL. 1993. The caracal, Felis caracal Schreber, 1776, as predator in the West Coast National Park. 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