CARNIVORES

Hans KruukInstitute of Terrestrial Ecology

I. Species DiversityII. Size and Ecology

III. Foraging and PhylogenyIV. Carnivore Guilds in EcosystemsV. Carnivore Social Systems

VI. Changes in Diversity

GLOSSARY

basal rate of metabolism The minimum amount ofenergy spent by an adult animal that has not eatenrecently, at normal body temperature during rest(usually sleep).

eutherian Mammal in which the embryo is attachedto the mother by a placenta

fissipedia suborder of the Carnivora with divided toes.guild Species in a community that use similar re-

sources.marsupial Mammal without placenta and with a pouch

to carry the young.monophyletic Derived from a single ancestor.pinnipedia Suborder of the Carnivora with fin-like

limbs (seals, sea lions, and walrus).plantigrade Walking on the soles of the feet.

CARNIVORES are a highly varied group of mostlyclosely related species. This article discusses the diver-

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sity of terrestrial carnivores, excluding the seals butincluding some marsupial species. Most of the terres-trial carnivores belong to one single order: Carnivora.Some of the taxonomic and evolutionary relationshipsare discussed as well as the social organizations, effectsin ecosystems, and conservation status.

I. SPECIES DIVERSITY

Among the mammals that are broadly referred to asCarnivores there is a weasel of approximately 45 g anda polar bear of up to 700 kg, approximately 15,000 timesheavier. There are species living almost permanently inwater (sea otter), in trees (palm civet), or in deserts(fennec fox); some eat buffaloes, some eat beetles, andsome eat bamboo. It is not surprising, therefore, thatwith such large variation and divergent adaptive fea-tures there is disagreement among researchers aboutthe evolution and classification of species. Classificationis based on morphological evidence (dental characteris-tics, anatomy of the skull base, and other morphologicalfeatures) and on molecular genetic information.

This article will deal with the approximately 230Fissiped carnivores, i.e., the terrestrial species of theorder Carnivora and excluding the seals, sea lions, andwalrus (Pinnipeds). It will also discuss a group of eco-logically rather similar species of marsupials in Austra-lia belonging to the families Dasyuridae and Thylaci-nidae.

The Carnivora are a monophyletic order, descended

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from the family Miacidae approximately 60 millionyears ago in the Palaeocene. The order has two mainbranches, the dog-like Canoidea and the cat-like Fel-oidea. The 33 seals and sea lions and walrus belongingto the Pinnipeds are sometimes included in the orderCarnivora and sometimes given separate status. Theyevolved from the Canoidea, but there is disagreementabout which terrestrial carnivores are their closest rela-tives, the main candidates being the bears and themustelids.

The Carnivora are generally divided into seven fami-lies, although some taxonomists recognize more. TheCanoidea include the Canidae (dogs) with 35 species,the Mustelidae (martens) as the largest carnivore familywith 67 species, the Ursidae (bears and pandas) with9 species, and the Procyonidae (raccoons) with 15 spe-cies. The Feloidea comprise the Felidae (cats) with 35species, the Hyaenidae with 4 species, and the Viver-ridae (mongooses and genets) with 66 species. Themain taxonomic disagreements are over the Ursidaeand the Viverridae. The two species of panda are oftenthought not to belong to the bears but to deserve aseparate family or they may be included with the Procy-onidae, and the Viverridae are often divided into twofamilies—the Herpestidae (mongooses, 31 species) andthe Viverridae (genets and civets, 35 species).

The dogs and foxes (Canidae) constitute a highlymonomorphic family. All are very dog-like with non-retractile claws, and all are coursing predators, such aswolves, coyote, jackals, foxes, wild dog, bush dog, andmaned wolf. All species have much in common in theirecology and social behavior, although they may varyfrom solitary to gregarious. Sizes vary between that ofthe large gray wolf (up to 80 kg) to that of the tinyfennec fox of little more than 1 kg. Canids occur onall continents, and with the dingo they even fielded anearly introduction in Australia. The gray wolf is theancestor of all domestic dogs.

Eleven canids (31%) are endangered or vulnerable,and all the large species are threatened in at least someparts of the world (the two wolves, African wild dog,and the Asian dhole).

The members of the marten family or Mustelidaeoccur in both the New and the Old World, with weasels,martens, mink, polecats, skunks, otters, badgers, andothers. There are relatively few species in Africa, per-haps because of competition with the similar viverrids.In Britain, there are three times as many mustelid spe-cies as members of all other carnivore families com-bined, and in the United States there are also moremustelids than others. Almost all are quite small ani-mals (45 g to 45 kg), with the largest species being

some of the 13 species of otters. They are usually slimlybuilt, some with retractile claws, and with a very distinc-tive bouncing gait, but the family is quite variable andsome species are stocky, such as the badgers. Also,in feeding and social behavior they vary greatly, fromsolitary predators on mammals to group-living animalsfeeding on earthworms or fish.

Stoats and weasels have been introduced on severalislands outside their normal range, and the North Amer-ican mink is now an abundant exotic in many placesthroughout Eurasia and South America. Some of themustelids are almost extinct (e.g., the black-footed fer-ret and the European mink), some were exterminatedrecently (sea mink), and several are in trouble (otters)or have just returned from the brink of extinction (suchas the largest of them all, the sea otter). However, onlyseven species (10%) are listed as endangered or vul-nerable.

The bears and pandas (Ursidae) are comparativelylarge and some are huge (weighing up to 700 kg),stockily built, plantigrade with nonretractile claws, andvery short tails. The exception is the very aberrant redpanda (a small arboreal species with a long tail), aspecies often classified as a procyonid. All but the polarbear are mostly vegetarian; they are solitary animalswith a fairly simple social organization. The bearsevolved more recently than the other carnivores andsuccessfully colonized areas as far apart as the drift icein the Arctic and the dense forests of the Old Worldand neotropics. Bears of colder regions hibernate. Morethan half of the species (five or 56%) are endangeredor vulnerable, and all are in trouble in at least part oftheir geographic range.

Members of the raccoon family Procyonidae are allrather long-bodied animals, relatively small (up to 8kg), with long, ringed tails, and they walk plantigradewith nonretractile claws. They occur naturally only inthe New World. In addition to the various species ofraccoon throughout the Americas, there are also otherNeotropical species, such as the coatis, the kinkajou,and the cacomistle. They are carnivorous and insectivo-rous as well as herbivorous. Their social behavior isquite variable; most are solitary but some, for example,female coatis, live in large packs. Also, common rac-coons may occupy winter dens in groups. None areclassified as endangered, although some raccoon speciesare known from only one or two islands, on whichthey may be rare. In several areas of Eurasia commonraccoons are now frequent as an introduced species.

The Viverridae are a large Old World family of smallanimals, occurring almost entirely in Africa and Asia.They are the most ‘‘primitive’’ carnivores, i.e., the closest

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relatives of the carnivores’ original forebears, the Miaci-dae. The family includes many species of genet andcivet, linsang, binturong, a large range of mongooses,meerkat, fossa, fanaloke, and others. Some taxonomistsrecognize the mongooses as a separate family—the Her-pestidae (otherwise classified as a subfamily Herpesti-nae). The mongooses are long-bodied and look some-what mustelid-like, with nonretractile claws; incontrast, the rest of the viverrids look and walk muchmore cat-like, with retractile claws. The fossa from Mad-agascar is unusually large (up to 20 kg), but all otherViverrids are much smaller, especially the mongooses.Most are solitary, but some mongooses and meerkatslive in large packs. Most of their food is invertebrate,but they also take small mammals, etc. and occasionalvegetable food.

Few viverrid species appear to be endangered (fouror 6%); of these four, three are on Madagascar, an islandbeset by deforestation problems.

The Hyaenidae have only four species left, despitea fossil record showing large numbers in the geologicalpast, and they occur only in the Old World. Three arerelatively large species of 50 kg or more and are typicalcoursing animals with a dog-like build and nonretractileclaws. Hyaenids are carnivorous; they often scavenge,although some also take vegetable food, and the small-est, the aardwolf, is a termite specialist. The largestspecies, the spotted hyena, is a gregarious hunter oflarge mammals, but the others are solitary. One of thefour, the brown hyena, is classified as vulnerable as aspecies, but in many countries the others are also en-dangered.

Finally, there are the Felidae, the proper cats, ahighly monomorphic family with many species. All arebuilt as stalking predators, with retractile claws, andthey range in size from fairly small to large, from servaland flat-headed cat and many other small species to lynxand tiger (up to more than 300 kg), various leopards,cheetah, and lion (up to 250 kg). All are carnivorous,but small species also eat many invertebrates. The socialorganization of all species is very similar—solitary andterritorial, with the lion as the only group-living excep-tion. Felids occur naturally on all continents exceptAntarctica and Australia. The wild cat Felis lybica hasbeen domesticated and it has been introduced virtuallyeverywhere in the world; it is now the most wide-spread carnivore.

There is concern about the conservation status ofalmost all cat species, especially the ones with desirablefur. Twelve (34%) are endangered or vulnerable, includ-ing all the large ones such as tiger, cheetah, jaguar, andvarious leopards, but not the lion.

The mammalian carnivore families outside the Car-nivora proper are the Australian marsupials Dasyuridaeand Thylacinidae. There are four dasyurid species thatare very similar to Carnivora: three quolls or, as theAustralians call them, ‘‘native cats’’ and the Tasmaniandevil. They are relatively small, with the quolls similarin size and appearance to martens or mongooses andthe Tasmanian devil more like a small badger in sizeand shape, and they are typically carnivorous, solitary,nonterritorial animals. The thylacine was the only spe-cies in its family and it was also the largest of thesemarsupial carnivores (comparable in size to a largejackal or coyote). It was exterminated very recently. Theother, dasyurid species now have very much reducedgeographical ranges and they are vulnerable.

II. SIZE AND ECOLOGY

There is a large diversity of sizes among carnivores,and the ecological implications of this variation areconsiderable. The basal rate of metabolism of carnivorestends to be greater than that of same-sized herbivores,and a large predator expends more energy than a smallone; therefore, it has to capture more prey. However,the increase in metabolism with size is not linear, andwhen expressed as energy requirements per kilogramof body weight a large predator is more efficient thana small one (Fig. 1).

FIGURE 1 Basal rate of metabolism (oxygen consumption per gramper hour at rest) in carnivores as a function of body mass. Reprintedfrom B. K. McNab, ‘‘Basal rate of metabolism, body size, and foodhabit in the order Carnivora,’’ in Carnivore Behavior, Ecology, andEvolution ( J. L. Gittleman, ed.). Copyright 1989 Cornell University.Used by permission of the publisher, Cornell University Press.

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The body mass of a carnivore, when combined withthe group size in which it lives, is correlated with thesize of its home range, although there is much variation(Fig. 2). Much of this residual variation is due to effectsof habitat and to differences in diet (predators of verte-brates having larger ranges than insectivorous ones).There is no significant correlation between body massand gregariousness, i.e., large carnivores are no morelikely to live in groups than are small ones.

Brain size of carnivores increases with body size.Irrespective of this, a meat-eating, hunting carnivore oran omnivorous species generally has a relatively largerbrain than an insectivorous one. Bears have relativelylarge brains, whereas Viverrids and Hyaenids have rela-tively small ones and the others have intermediate-sized brains.

In general, large carnivores take larger prey than dosmall ones, but there are important variations. First,

FIGURE 2 Home range size of carnivores as a function of metabolicneeds. �, Canidae; �, Ursidae; �, Procyonidae; �, Ailuridae; �,Viverridae; �, Mustelidae; �, Felidae; �, Hyaenidae (reproducedwith permission from Gittleman and Harvey, 1982. Carvinore home-range size, metabolic needs and ecology. Behav. Ecol. Sociobiol. 19,57–63, Fig. 1, Springer-Verlag).

some of the largest (bears) are mostly vegetarian. Sec-ond, the trend varies between carnivore families. Withinthe mustelids there is a nonsignificant negative correla-tion between predator body mass and prey size, so thepredator–prey size principle does not apply. Both felidsand canids show a strong positive correlation, but theslope of the relationship is different: The increase inprey size with predator body mass is much steeper infelids (Fig. 3).

There are many specific deviations from the pre-viously discussed general patterns, but the trends aresignificant. Greater energetic demands on larger carni-vores are met by a dependence on larger prey, whichis likely to make the large predators more vulnerable.Many of the larger carnivores are threatened globallyor in parts of their range, e.g., many of the large spottedcats and the tiger, wolves, and hyenas.

III. FORAGING AND PHYLOGENY

The diet of carnivores in general, and that of theirmarsupial equivalents in Australia, consists of verte-brate prey but also invertebrates and vegetable matter.The order Carnivora shows dental specializations en-abling easy digestion of vertebrates, such as large ca-nines and the carnassial shear, but in several speciesthe molars have been further adapted to a more grindingfunction when eating plants.

Foraging or hunting behavior of carnivores consistsof variations on a general theme. A search leads todetection and selection of a potential victim or othersource of food, and it is followed by an approach whichmay contain elements of stalking and/or chasing. Theactual capture of prey may include seizure, immobiliz-ing, and killing, and this is followed by eating, takingfood to cubs, or sometimes quietly caching it for laterconsumption. Parts of this sequence may be absent,and in fact most carnivores will just search and theneat small food items without much further ado. How-ever, even if there is a full-blooded hunt, some speciesnever stalk (e.g., dogs or hyenas), others never chase(e.g., cats), and some may not show any specific killingbehavior but just eat (e.g., hyenas).

The chain of events aimed at the capture of preymay be broken off at any stage depending on circum-stances; it can also be started at any stage. It is highlyadaptive, depending on prey and environment, withthe predator’s own motivation (its degree of hunger)apparently affecting especially the early searching stagesof the hunting sequence.

Conspicuous in the predatory behavior of many car-nivores is the phenomenon of surplus killing, i.e., kill-

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FIGURE 3 The relationship between size of predator and prey. For each species of carnivore, mean body weightand main food category are given. 1, invertebrates; 2, small rodents; 3, rabbits and hares; 4, larger mammalsless than 50 kg; 5, mammals more than 50 kg (reproduced with permission from Kruuk, 1986).

ing more than is required for immediate consumption.Classic examples are the fox in the hen house or gullcolony or a lion among a cattle herd; it has been de-scribed for hyenas, polar bears, wolves, leopard, andothers. Large numbers of animals were killed withoutbeing eaten. All these situations have in common a lackof defense by the prey: The prey may be immobilizedby particular weather conditions, it may be penned in,or it may have lost its antipredator defense throughdomestication. In these cases, the predator is sated andno longer hungry, but hunger normally affects only theearly stages of the carnivore hunting sequence, espe-cially the search. If, for some reason, no search or stalkor chase is needed because the hunter suddenly findsitself close to the quarry, then the rest of the huntingsequence is put in train irrespective of hunger, andthere is no inhibition to capturing and killing. Function-ally, such events are wasteful from the carnivore’s pointof view because they reduce prey availability withoutthe predator getting the benefits.

Food caching (i.e., the storage of food in a hiddenplace) is a behavior pattern that limits this waste andutilizes the consequences of surplus killing. Many spe-cies do it, and do it in many different ways. In all canidsit is highly stereotyped: A small hole is dug, and onesingle prey is dropped into it and covered with earth

or vegetation by sweeps of the snout. In other familiesthere are many variations on the caching theme: Leop-ards take a carcass high into a tree; spotted hyenascache chunks of food in shallow water; brown andstriped hyenas push it into a dense bush; stoats, mink,and other mustelids may make large stores by draggingnumbers of prey into a single hole; wildcats may putremains of their quarry under a log; and some of thelarger cats may civer a carcass with vegetation. Themethods are consistent within the species, for canidswithin the family, and for martens within the subfamily,suggesting that caching has evolved in carnivores onseveral different occasions. There is no evidence of cach-ing for the procyonids or viverrids, nor is it done bythe marsupial carnivores.

Although food caching may use some of the surpluskills, it still does not utilize all the apparent waste.Not only are some of the caches never revisited by theperpetrator but also in the larger surplus kills only asmall proportion of the victims are stored. There maybe scores of dead gulls left by a fox and of gazelleleft by spotted hyenas. In some carnivores caching isparticularly highly developed. For instance, foxes areable to remember where they stored what, and theyreturn preferentially to the more desirable cached items.Foxes also use some kind of bookkeeping system for

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their caches, leaving a drop of smelly, long-lasting urinenear those caches which they have emptied.

Foraging and hunting behaviors are features thatdiffer with the phylogeny of the predator. Canids invari-ably are coursing and running predators, with an occa-sional semistalking approach of prey, and they oftenforage by ‘‘sniff and search.’’ At the other extreme, felidssearch almost entirely dependent on vision and theyapproach their quarry in a highly concealed stalk orambush. Most members of the other families, includingthe marsupial carnivores, show the canid sniff andsearch behavior pattern. Only the genets and civets havea stalking behavior that is similar to that of the felids.

When a relatively small vertebrate prey is caught,the felids, many of the mustelids, and civets will kill itby severing the spinal cord with their canines. Canidsalso have a specific killing method—violently shakingthe prey. Felids kill large prey with a throat bite, orthey suffocate it with a bite over the nose and mouth.In almost all other predator–prey interactions thereis no specific killing or immobilizing behavior—thepredator just eats the prey. Most species of carnivorehave highly specific ways of dealing with a prey and itscarcass, and it is often possible to distinguish afterwardswhich predator was responsible for a kill.

Some subfamilies have evolved extreme foraging spe-cializations. The Lutrinae (otters) dive for fish and crabsusing their tactile senses, but essentially their huntingis also based on the canid pattern. Several Melinae andMellivorinae (badger) species pursue their prey by dig-ging after it. Species such as the otters and African wilddogs use energetically demanding behavior to catchtheir quarry (a high investment and high reward strat-egy), which makes them especially vulnerable to fluc-tuations in prey density and to food loss to scavengers.

As a result of the variation in foraging methods be-tween families and subfamilies, there are also phyloge-netic patterns in the diet. Compared with many otherspecies of mammals and birds, diet analysis for carni-vores is relatively easy, although it has some seriousproblems. Food usually consists of clearly discreteitems, which can be recognized and quantified. Further-more, scats are often easy to find, no matter how elusivethe animals may be, and scat analysis has become amajor tool despite the difficulty of relating scat contentto diet in a quantitative manner. Also, for many speciesit has proved possible to obtain direct, quantitative ob-servations of predation and foraging behavior. The re-sult is an extensive body of knowledge of carnivorediet, the important link in the relation between thepredators and their environment.

One summary showed that of 111 species of carni-

vore (from all families), only 36% could be classifiedas predominantly meat eaters, i.e., taking more than60% of their diet in the form of other mammals orbirds. Indeed, in that analysis among representatives offamilies such as the bears, raccoons, and viverrids, therewere no proper meat eaters at all, and they were foundto feed on insects, vegetation, or a mixture of variousfood categories. Many species were called omnivorousif their diet did not include 60% of any one categoryof food. However, such a limit is quite arbitrary, andmany important species were left out of the analysisbecause of lack of information. Therefore, it is an over-simplification, and one could also summarize the dietdifferently (Fig. 4): The majority of carnivore specieswill eat meat and will prey on other mammals at sometime or other. However, the point had to be made thatmany other kinds of food are involved.

There is a clear importance of phylogeny in the diet:The food of a felid tends to be more like that of anotherfelid than that of a canid and vice versa, and this appliesto several families (Fig. 4). All families except the felidsare intensive exploiters of vegetable and invertebratefood sources: The Felidae are the most exclusively car-nivorous—the ultimate predators. Only the felids, hy-aenids, and canids feed significantly on large mammals,with an occasional exception in the other families. Theviverrids, which are probable ancestors of felids andhyaenids, do not kill larger mammalian prey but theyare either insectivorous or have a very mixed diet. Thediets of the four hyenas are more different from eachother than between the members of the other families,and their specializations range from wildebeest to ter-mites or melons or carrion. The bears and pandas arevegetarians. Species in the raccoon family all have amixed diet, including much vegetable matter. Canidshave mostly varied diets, composed of insects, fruits,and mammals. Many of them are proper meat eaters,but even these often include some vegetable matter,quite unlike the cats.

Some of these family-specific trends are further re-fined in the subfamilies. The mostly meat-hunting mus-telids also include two subfamilies with 9 badgers,which almost all feed on invertebrates and vegetation,and a subfamily of 13 otters that subsist on fish or crabs.

Not only are there differences between families andsubfamilies in the kinds of prey or vegetation whichthey select, but also the degree of specialization varies(Fig. 5). Specialization can affect an animal’s vulnerabil-ity to environmental change. Among the canids, eachspecies uses an average of 6.5 (out of 10) major preycategories, each constituting at least 1% of its food. Onthe other end of the scale, each bear only uses 3.7 prey

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FIGURE 4 The use of different foods by species from different families. Percentage of species ineach family in which a particular food category constitutes more than 1% of diet. Veg, vegetablefoods; inv, invertebrates; amp, amphibia and reptiles; rod, small rodents; lag, rabbits and similarsize prey; s.mam, large mammals smaller than 50 kg; l.mam, large mammals larger than 50 kg;car, carrion (reproduced with permission from Kruuk, 1986).

categories and each felid 4.0, so they are much morespecialized. The other carnivore families are intermedi-ate. This specialization (dependence on a few resources)may make bears and felids more vulnerable to environ-mental change than canids.

The degree of specialization can be described onlyin the broadest of terms because it is difficult to measure

and quantify. Terms such as omnivore, opportunist,generalist, and specialist have no absolute values, andthey refer to animals which may be selecting from avariable set of availabilities. There is also a problemwith definitions. For instance, the Eurasian badger ishighly focused in its food selection in any one area,concentrating entirely on earthworms in northwestern

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FIGURE 5 The number of food categories used by species of different carnivore families. N,number of species studied, with mean and standard deviation of the number of major foodcategories (see also Fig. 4) (reproduced with permission from Kruuk, 1986).

Europe, on rabbits in southern Spain, and on olives innorthern Italy. There is no doubt that in each of theseareas badgers are highly specialized, but their specializa-tions are different in different places and overall theycould be described as opportunists. Currently, there isno good quantitative descriptive term for such a pattern.

Nevertheless, despite inadequate terminology it isrecognized that in any one place some species use manymore different prey categories than others. For instance,a cheetah on an African savanna takes almost only smallor medium-sized ungulates on open grasssland,whereas a leopard in the same area is much more catho-lic in its tastes. It eats the same mammals but also muchsmaller mammals as well as birds and snakes, stalkingthem in the open and in dense bush or between therocks. Along European streams a mink will eat smallmammals, frogs, fish, birds, and insects, whereas alongthe same banks the (larger) otters feed almost exclu-sively on fish and frogs, clearly much more focused.Such a broad comparative indication of specializationsuggests the dependence of a predator on few or manyprey categories, even though there may be difficultieswith labeling as specialist or opportunist.

In general, because closely related animals often havesimilar food habits, food selection may be termed a

conservative characteristic in the evolution of carni-vores. There are many exceptions; for instance, amongthe meat-hunting felids there is a fishing cat, and thehyena family includes the aardwolf, which feeds onnothing but termites, the spotted hyena, which is anexclusive large ungulate hunter or scavenger, and thestriped and brown hyenas, which are as catholic in theirtastes as possible. However, these exceptions do notinvalidate the overall importance of ancestry in theanimals’ environmental relationships.

IV. CARNIVORE GUILDSIN ECOSYSTEMS

Closely related members of the same carnivore familytend to exclude each other, although there are impor-tant and puzzling exceptions. Of course, competitionbetween natural populations of different carnivores israrely observed, probably because those cases in whichit occurred have long ago come to their natural conclu-sion, i.e., the demise of one of the contestants. However,when perturbations occur competition may be obvious.

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For instance, the introduction of the American minkin Europe totally removed the European mink frommost of its range. The famous wolf population of IsleRoyal arrived there in the early 1950s, and it completelyreplaced a population of coyotes. There are several ob-servations of wolves killing coyotes, apparently withoutthe coyotes being eaten. In many other areas in NorthAmerica, just one of the two species is found, althoughusually these places would appear to be suitable forboth. Coyotes tend to replace red foxes.

Red foxes are aggressive to arctic foxes and excludethem when their areas overlap, but arctic foxes can feedand survive at much lower temperatures. Recent redfox increases (e.g., in northern Scandinavia) caused thedemise of arctics over large areas. In the 1970s, whenthe black-backed jackals of the Serengeti were deci-mated by disease, the very similar and previously rareside-striped jackal population increased dramatically.Tigers are reported to often exclude leopards, and differ-ent species of otters exclude each other.

Also, species that are not closely related but haveoverlapping ecological niches may affect each other.For instance, the African wild dog disappeared fromthe Serengeti between the 1960s and 1990s probablypartly because of an increase in populations of hyenasand lions.

Exceptions to this pattern of exclusions are the threespecies of African jackal. They are very similar andclosely related; nevertheless, their geographical rangesoverlap considerably and they can be seen eating fromthe same carcass.

There are other examples of perturbations or speciesintroductions causing the disappearance of competingcarnivores, but such events are relatively rare. Thus, itis often assumed that populations of predators each

FIGURE 6 Even spacing of mean lengths of skulls of Mustelid species in Britain and Ireland, log scale.The mink has recently been introduced (reproduced with permission from Dayan and Simberloff, 1994).

have their own ecological niche and rarely affect eachother. However, the ecosystems that we see are endresults, and often what we see may be the status quolong after earlier populations have been wiped out orhave been prevented from moving in.

One way in which predator species adapt to an eco-logical niche in a particular habitat is through morpho-logical or behavioral variation. When potentially com-peting species share a range, differences between them(e.g., in size) may be greater than those from animalsthat live in ranges not shared with the other species.This is known as character displacement. One of itsconsequences is that in a guild of predators in any onearea a character, such as body size or size of the canines,shows a fairly evenly spaced stepwise distributionamong species (Fig. 6). The obvious effect of this is tominimize competition. Such divergence of morphologi-cal characters does not always occur, however, and itsstriking demonstration in British mustelids is con-trasted with an almost absence in Serengeti jackals. Themarsupial carnivores of Tasmania also show a clearcharacter divergence.

The existence of such structured mechanisms, toavoid competition within predator guilds in ecosystems,suggests that resources for the carnivores may be at apremium. This in turn presents the possibility that thepredators depress prey populations.

It is often argued that predators have little or noeffect on prey numbers, as demonstrated by ecosystemssuch as the Serengeti with more than 25 carnivore spe-cies that coexist with the many prey in apparently stablepopulations. However, such an apparent stability is theresult of interactions over a long period of time, and itis possible that many prey species were extinguishedin the past and many predator–prey relationships have

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not had a chance to become established (as first arrivalsin the ecosystems were eliminated).

The deliberate or accidental introduction of carni-vores into ecosystems in which they were previouslyabsent provides an opportunity to demonstrate effectsof predation. Introduced predators (cat, dog, red fox,mongoose, American mink, stoat, and ferret) havecaused extinctions and declines of endemic prey speciesthroughout the world, including many birds, mammals,and reptiles. There is little doubt, therefore, that carni-vores cause extinctions or prevent populations frombecoming established, and they must have done so inthe evolutionary past. On all continents the fauna wouldlook very different from what it is now if there hadbeen no carnivore predators.

Also in the predator–prey systems which currentlyexist, the effects of carnivore predation can be far-reach-ing. Predator removal often dramatically increases num-bers in prey populations compared with those in suit-able control sites, as demonstrated by foxes preying onpartridges. Pest species such as rabbits can be limitedin numbers by carnivores operating in conjunction withother mechanisms such as disease. Wolves may exercisemajor effects on populations of caribou, moose, andwhite-tailed deer, and spotted hyenas can have a majoreffect on wildebeest. Often, other limiting factors areinvolved simultaneously, e.g., predators may be themeans whereby a herbivore population is maintainedat the carrying capacity of the vegetation.

V. CARNIVORE SOCIAL SYSTEMS

The majority of carnivores are solitary and territorial.Their spatial organization is maintained by females(with or without offspring) defending a range againstother females of the same species, and by males de-fending a (larger) range against other males. Maleranges may overlap with several females ranges. Territo-rial behavior involves scent marking and visual displaysas well as direct aggression.

There are some important variations to this general-ization. The marsupial carnivores are not territorial;therefore, instead of a regular spacing between individu-als, they are more or less randomly distributed. Thisbegs the question, not satisfactorily answered to date,why eutherian carnivores spend so much time and efforton risky territorial behavior if other species with similarecology can do without.

The organization of canids is pair based rather thansolitary; a male and a female share the same range. Thisis also the only family in which males usually assist in

providing the offspring (by regurgitating food). Thefact that such pair behavior is tied with the species’phylogeny suggests that in individual species it is notnecessarily adaptive.

From the simple, territorial arrangement a grouporganization has evolved independently in several spe-cies in all carnivore families except the bears, and suchgroup living has complicated land tenure considerably.Among the canids the most striking examples are thewolf, the wild dog, and the dhole in Asia, but in severalother canid species offspring may also remain for 1 or2 years, overlapping in time with subsequent litters ofthe basic pair. This has been described for several jack-als, foxes and others.

African wild dogs live in extremely tight packs, oftencomposed of 20 or more individuals, almost alwaysclose together, with on average twice as many adultmales as females. The wolf has a very different organiza-tion. It also lives in sometimes large packs, but it doesso in a much more ‘‘fission–fusion’’ type of society, withindividuals coming and going, sometimes hunting ingroups and sometimes alone, within the pack territory.In both species usually only one female per pack breeds.

Group organizations in other carnivore familiesshow as many different patterns as there are species,with, for instance, lions in permanent prides of up to20 related females joined by small groups of maleswhich are replaced every few years. Spotted hyenaslive in female-dominated clans of up to 80 in groupterritories, and individual members may hunt or joinwith others or they may be solitary within the groupterritory. Cubs are cared for almost entirely by theirown mothers. Both banded and dwarf mongooses occurin dense packs, with the sexes mixed, and all membersof the pack care for all offspring, Eurasian badgers for-age on their own and look after their own cubs only,but they live in group territories defended by both sexes.Female Eurasian otters, on the other hand, may occupyindividual core areas within a group territory of five orsix females, whereas males remain in their own ranges.

For the phenomenon of group living in carnivores,there are no striking, simple phylogenetic trends andno substantial effects of body size, climate, prey size,predation, or various other factors to explain the occur-rence of packs, bands, or prides. It does not appearthat social species have done any better or worse thansolitary ones in terms of numbers or densities, nor istheir future survival more or less endangered. There is,however, one set of environmental factors which appearto affect gregariousness, i.e., the distribution of food orof resources in general.

Currently, there is only one general hypothesis to

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explain grouping of carnivores—the resource disper-sion hypothesis, first explicitly presented by Macdonald(1983). In principle, it relates the size of territories andthe numbers of animals inhabiting each territory to thespatial and temporal pattern of resources. For instance,it suggests that badgers in northwestern Europe live ingroups because their main food, earthworms, occurs inwell-spaced patches, each of which is available only atcertain times. To be able to feed at all times a badgerneeds a large area with several patches, with the sizeof the area determined by the scatter of the patches.Once a badger has such a territory it can accommodateseveral more individuals with only limited or no compe-tition. The hypothesis is attractive, but it does not ex-plain all the intricacies of spatial organization. To date,there is no comprehensive alternative.

Carnivores living in groups may or may not huntcooperatively, depending on species or conditions.Clear advantages of cooperation, in terms of huntingsuccess or energy balance, have been demonstrated forwild dogs and spotted hyenas. Lions collaborate on awell-organized basis, with each pride member occu-pying a preferred place in the hunting formation anddeviations of this pattern resulting in lowered success.

VI. CHANGES IN DIVERSITY

When the Carnivora first appeared, approximately60–40 million years ago, there were other, similar ani-mals already well established. For instance, the extinctorder Creodonta included families such as the Hyaeno-dontidae, and there were various large marsupial preda-tors such as the Thylacoleo or pouch lion. Proper car-nivorous feeding and predation have evolved severaltimes independently—at least twice among the marsu-pials (in the Borhyaenidae in South America and someDasyuridae in Australia) and twice among placentalmammals (in Creodonta and Carnivora).

The large carnivorous expansion from the Palaeo-cene onwards coincided with the evolution of angio-sperms, flowering plants and grasses (evolving awayfrom the ferns and gymnosperms such as conifers).This resulted in a large floral diversification, includingsavanna-type vegetations, and enabled the extensive di-versity of ungulates and rodents to evolve. This in turnenabled the evolution of specialist predators.

Most of the other, noncarnivore large predators havenow gone extinct, with the last creodonts occurringapproximately 8 million years ago and the last reallylarge marsupial carnivores occurring 2 million yearsago, when species of Homo were already well estab-

lished. Of the smaller marsupial carnivores, just a fewsmall dasyurids still occur in Australia. However, whilethe other predators slowly disappeared, the order Carni-vora diversified into a multitude of different families,genera, and species.

Why the creodonts disappeared, while at least ini-tially carnivores thrived and probably replaced the creo-donts, is a mystery. Creodonts and carnivores wereclosely related and the skeletal remains, such as verte-brae and the locomotory system, were similar. The dif-ference between creodonts and carnivores was notmuch greater than the variation within these groups.However, obviously there is more to an animal than itsskeleton, and the reasons for extinction may well havelain in other aspects of morphology, physiology, orbehavior.

In the early stages of evolution the advantages appearto have lain with the creodonts, and only after 20 mil-lion years did the balance tip in favor of the Carnivora.The Carnivora have been four times as successful asthe creodonts: The latter are known from 45 generaspanning approximately 45 million years, whereas Car-nivora, excluding living and aquatic genera, are knowfrom 218 genera over a span of more than 55 millionyears.

Carnivore species are also fewer now than they werein the geological past. In fact, most of the Carnivorahave become extinct, and although there is still a richcomplement of species, there were many more in thepast. For instance, we know of 333 genera in the sevenextant families of carnivores, of which 237 (71%) areextinct. Many complete carnivore families have alsodisappeared, just like the creodonts and large marsu-pial predators.

An interesting phenomenon was the occurrence ofsaber-tooth species. Saber teeth evolved several timesindependently in different species, families, and evenorders and included the Megantereon, Homotherium,and Machairodus, which were at least as big as a lion,and formidable felids such as the North American saber-tooth cat Smilodon. Some of these were present at thesame time as early species of Homo, but all of them areextinct. They pose a difficult problem to paleontolo-gists. Large canines are used by today’s carnivores forkilling prey and for social purposes such as fightingopponents over territorial claims. However, were theextra-large saber teeth—the huge, flat daggers whichwere seemingly far too large for any jaw—used to killextra-large prey, for opening carcasses, or what? Infossil assemblages it was always the very largest ones,the top predators, which sported saber teeth.

There is no likely explanation for saber teeth in the

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acquisition of food. The fragile, sharp weapons, oftenwith serrated inner edges, must have been quite uselessagainst thick skin or on large bodies, with the gapeof the owner being insufficient to use these canineseffectively. However, saber teeth were obviously effec-tive weapons; otherwise, they would not have evolvedseveral times independently. However, they also disap-peared again in all these cases. It is likely that saberteeth made use of some Achilles heel in their prey (ofwhich we have no evidence today), but that in responsethe prey species evolved means of protection. It was anarms race which was eventually lost by the sabers, butwe do not know who conquered and why.

Homo is a highly successful hunter, and mankindwas and is in competition with Carnivora at severaldifferent levels. Homo also preys on and is preyed on byCarnivora. Therefore, are people the cause of carnivoreextinctions? The question is often asked, and answersare far from straightforward. Many carnivore speciesextinctions occurred approximately 4 million years ago,at the time that hominids arrived on the scene, andmany followed during the next 2 million years.

However, many extinctions occurred before man ar-rived, and at the time Homo’s arrival was not the onlyevent which changed the environment. There weredrastic changes in climate, for instance, approximately3.2, 2.4, and 0.8 million years ago. The PleistocenePeriod started at 0.8 million years ago with a massiveclimatic shift that coincided with the appearance inEurasia of African species such as the lion, leopard,spotted hyena, and perhaps the major (although notthe first) movement out of Africa of Homo. If suchmajor dispersal events occurred in conjunction withclimatic changes, it is equally likely that extinctionswould have occurred.

For many of the carnivore extinctions, we cannotblame our own species with any conviction. Homo mayhave been closely involved or not at all, and perhapsenvironmental change rendered species more vulnera-ble to competition and predation by mankind. Ofcourse, recent extinctions have been fairly well docu-mented, and here mankind’s guilt is in no doubt. TheTasmanian wolf or Thylacine was exterminated bysheep farmers in the 1920s and 1930s. The North Amer-ican sea mink was obliterated in the late nineteenthcentury for its fur, and the sea otter almost followed itinto oblivion; it was barely saved and it has recoveredfairly well. The ‘‘wolf ’’ of the Falkland Islands was still

there when Charles Darwin visited, but sheep farmersexterminated it and since the 1880s it has existed onlyin museums. Several carnivores were totally eradicatedfrom Britain, including the brown bear and the wolf,whereas wildcat, polecat, and pine marten have onlyjust managed to survive. There are long lists of carnivoreextinctions from throughout the world, and there is nodoubt that most of these were man induced.

Whatever caused the demise of carnivore species inthe past, it is important to prevent it from occurring inthe future. Several species are on the brink of extinctionin the wild, including tiger, panda, European mink, andblack-footed ferret, and many more face local extermi-nation. In geological terms, the diversity of carnivoresis decreasing extremely rapidly.

See Also the Following ArticlesFOOD WEBS • MAMMALS, BIODIVERSITY OF • PREDATORS,ECOLOGICAL ROLE OF

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