Some Aspects of Social Behavior in the Canidae. Zoological Society of London, London, N.W. 1, England

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1 AM. ZOOLOCIST, 7:65-7 (967). Some Aspects of Social Behavior in the Canidae DEVRA G. KLEIMAN Zoological Society of London, London, N.W., England SYNOPSIS. Despite the diversity of morphology and ecology in members of the Canidae, social behavior remains similar throughout the Family. Some specializations have occurred in groupliving species, serving to maintain group cohesion and to reduce intraspecific aggression, and these changes in behaviors and postures have been ones of degree rather than kind. The type of specialization differs in each species and is probably related to its ecology. Thus, the bateared fox has developed contact behaviors such as social grooming while the wolf has evolved more specialized agonistic postures that are used in the maintenance of a social hierarchy. The members of the Canidae, the dog and fox family, are diverse in their habits and widespread in their geographical range. They occur on every continent with the exception of Antarctica. Inhabiting the tropics, the desert, the Arctic, and the temperate regions, they range in weight from a few pounds to well over one hundred pounds and eat anything from large game to insects and fruit. This diversity of habits is the result of a lack of specialization and a built-in ability to adapt to environmental changes. The Canidae are opportunistic animals. For example, the coyote, in this century, has expanded its range and increased its numbers while many other carnivores of a similar size have become rare (Mech, 96). Similarly, the red fox is surviving in England despite the density of the human population and the loss of the majority of the rabbit population through myxomatosis. Many now live by scavenging on the outskirts of towns and making fruit a regular part of their diet. The factors, then, which have enabled the members of the Canidae to survive and even thrive are adaptability and non-specialization. This has decidedly affected their behavioral repertoire, so that social behavior and its expression through postures and movements is similar throughout the family despite important ecological differences. Most of the existing behavioral differences are ones of degree rather than kind. The purpose of this study was to examine these similarities and differences in social behavior in order to gain as broad a picture of the entire Family as possible. It (65) was hoped that this approach and the material gained from it would be of use in two ways. First, it would aid in the taxonomic classification of the Canidae by adding behavioral data to the existing anatomical data. Secondly, it was hoped that a latitudinal study would place the analysis of the behavior of single species such as the wolf or the red fox in a broader context. The results of the numerous behavioral and ecological studies of the wolf reported in this symposium could become more meaningful when comparisons are made with other members of the Family. ANIMALS AND METHODS Fifty-six specimens of the Family were available for observation. Table divides these animals into species and sexes as well as providing some field data on their social organization and hunting habits. The taxonomic classification followed is a compilation from several sources used in Morris (965). Most of the specimens observed were on permanent exhibition in the Zoological Gardens of the Zoological Society of London. The animals were mainly housed in large outdoor enclosures ranging from 6' X ' to ' X ' in size. These paddocks had a substrate of sand and pebbles. Several wooden posts were randomly distributed throughout the paddocks and were used by the dogs and foxes as scent-marking posts. All of the outdoor enclosures had adjoining inner dens to which all animals had access. The wolves, a pack of nine animals, were Downloaded from on 07 June 08

2 66 DEVRA G. KLEIMAN Species TABLE Cnninae. Wolf. Canis lupus. Coyote Canis latrans. Dingo Canis familiaris New Guinea singing dog Canis familiaris 4. Side-striped jackal Canis adustus 5. Black-backed jackal Canis mesomelas 6. Paraguayan fox Dusicyon gymnocercus 7. Maned wolf Ciirysocyon brachyurus 8. Raccoon dog Nyclereutes procyonoides 9. Red fox Vulpes vulpes 0. Arctic fox Alopex lagopus. Fen nee fox Fennecus zerda Simocyoninae. Cape hunting dog Lycaon pictus. Bush dog Speothos venaticus Otocyoninae 4. Bat-eared fox Otocyon megalotis. Members of the Canidae observed 7 this study. Sexes & ] 5 9 Ecology Hunt large game in packs in Northern Hemisphere (Young and Goldman, 944). Hunt medium-sized game singly and in pairs on plains of North America (Young and Jackson, 95). Hunt medium-si/.ed game on plains of Australia (Marlow, 96). Domestic dogs in New Guinea (Hargreaves, pers. conrai.). Scavenge; hunt small game singly or in pairs; also packs in forests of S. Africa (Van der Merwe, 95). Scavenge; hunt small game singly or in pairs in open veld of Africa (Van der Merwe, 95). Hunt singly or in pairs in S. America (Cabrera, 940). Hunt small prey singly over savannahs of S. America (Krieg, 940). Have varied diet; hunt in pairs or family groups in forests of Europe and Asia (Novikov, 956). Have varied diet: hunt singly in Northern Hemisphere (Novikov, 956). Hunt small game singly or in pairs in the tundra of the Arctic region (Ognev, 9). Prey upon small game and insects in desert of N. Africa (Schmidt-Nielsen, 964). Hunt large game in packs in savannahs of Africa (Kuhme, 965). Prey upon medium-sized game in packs in forests of Central and South America (Cabrera, 940). Prey upon small game and insects in groups in S. and E. Africa (Van der Merwe, 95). housed in a very large enclosure with two concrete shelters simulating underground dens. The substrate was earth and pebbles, and there were many large and small trees growing within the area. The members o the smaller species such as the red and Arctic foxes were provided daily with ground horsemeat, and two or three times weekly with fruits and freshly killed chicks and mice. Chunks of horsemeat on bone alternating with freshly killed rabbits were fed to the larger species such as the wolf. All animals were given a supplement of vitamins. Observations were carried out in front of the cages. Most individuals seemed to adjust to the presence of the observer, but a blind was utilized if individual animals were either extremely shy of, or overly friendly to, the observer. Few controlled experiments were possible because the animals were exposed to the public, were few in number, and the group size was different for each species. It was, however, possible to take advantage of changes arising from the transfer, death, or arrival of animals, and in certain cases to introduce temporarily two members of a single species which were housed separately. Despite the problems arising from the Downloaded from on 07 June 08

3 study of captive animals, most of the available field data on social organization and behavior in the Canidae were confirmed by the author's observations on zoo specimens. For example, a male and female Cape hunting dog without previous experience of each other were introduced and were playing within a few hours. A male and female maned wolf, on the other hand, which had several months experience of one another through sound, smell, and vision, but not physical contact, have not as yet been introduced successfully. The results of these two similar situations confirm reports that the maned wolf is a solitary animal (Krieg, 940) while the Cape hunting dog is unusually gregarious (Kiihme, 965). RESULTS The social organization of members of the Family varies from the solitary maned wolf to the communal Cape hunting dog. There is a gradation in sociability from the solitary species which are more fox-like to the social species which are more dog-like. This is a generalization and refers only to presently existing species. It implies nothing whatsoever about the evolution of the Family as a whole since insufficient data exist about the phylogenetic relationships within the Family. A most interesting exception to this generalization is the grouporiented bat-eared fox. General social behavior. Sociability in members of the Family is expressed in the amount of close physical contact and communal involvement in such behaviors as hunting and feeding, sleeping, and resting. Communal vocalizations, social grooming, and play are also found more often in the social animal. In gregarious species, this togetherness exists throughout the year and is not restricted to the breeding season. Species-specific differences are found mainly in the frequency of occurrence of these behaviors. Bat-eared foxes are often observed allogrooming, playing, and sleeping and resting in contact, while red foxes, although showing such behavior occasionally, usually move and act quite independently of one another. SOCIAL BEHAVIOR IN THE CANIDAE 6/ Communal hunting is uncommon in members of the Family. It is reported for wolves, dingos, Cape hunting dogs, bush dogs, and dholes (dhole, Sosnovskii, 967). Side-striped jackals are also said to hunt occasionally in groups. The remainder of the Family all hunt small game individually or in pairs and do not possess the cooperative hunting which we find in the wolf. Communal feeding occurs in the pack hunter, but also in the jackals and coyotes who as scavengers congregate at the kills of other large carnivores. Communal feeding is most ritualized in the Cape hunting dog where it has assumed an important role in the maintenance of social cohesion within the pack. After a kill, the adults will eat and partially digest the food. Both adults and young will then repeatedly induce others to regurgitate their meat by using a specific begging posture derived from infantile begging (Kiihme, 965). Raccoon dogs and bat-eared foxes regularly engage in bouts of social grooming, while this behavior only appears rarely in members of other species and then only between pairs during the breeding season. In the bat-eared fox, allogrooming has assumed such importance that there is a facial expression used to elicit grooming from conspecifics. The importance of mutual grooming of the face in the raccoon dog and bat-eared fox may be related to the fact that both species possess a black facial mask similar to the facial markings of the raccoon. Sleeping and resting in contact with one another occurs occasionally in the members of most species; it is observed regularly only in the raccoon dog, Cape hunting dog, bush dog, and bat-eared fox. Communal howling is found in the wolf, coyote, dingo, and New Guinea singing dog. Social howling has also been reported for the golden jackal (Seitz, 959). In wolves, coyotes, and golden jackals, the animals group together and greet one another before and during a howling session. There are thus elements of both physical and vocal contact present in the howl. Dingos and New Guinea singing dogs, on the other Downloaded from on 07 June 08

4 68 DEVRA G. KLEIMAN hand, are rarely in contact with one another although they howl in close proximity. In other species, e.g., the manecl wolf and Arctic fox, vocalizations often are emitted alternately by individuals and seern to be used for maintaining auditory contact with conspecifics from a distance. Sexual behavior. Sexual behavior was observed in seven of the nine species in which both sexes were present. These comprise the wolf, coyote, dingo, and New Guinea singing dog, raccoon dog, Arctic fox, bush dog, and bat-eared fox. There were few species-specific differences in the courtship behavior of the males. They would follow the female, sniffing and licking the vulva. This would be interspersed with mounting and pelvic thrusting in attempts to gain intromission. Little courtship play was observed. Females differed mainly in the degree to which they were receptive to the male, but comparisons cannot be made of these individual differences. With one exception, none of the females showed courtship postures which were significantly different from those of the domestic dog. The bush dog female possessed a standing posture more similar to lordosis in the cat than to the typical bitch. While being pursued by a male during her period of receptivity, she would lower her forequarters to the ground and hold her hindquarters and tail raised. At times, her ventral surface would be touching the ground completely. Copulations were observed in the coyote, dingo, and New Guinea singing dog, raccoon dog, Arctic fox, and bat-eared fox. All possessed the characteristic copulatory tie which lasted from two to twenty minutes. The tie is also known to occur in the wolf, maned wolf (Scherpner, pers. comm.), red fox (Tembrock, 957), and the dhole (Sosnovskii, 967). The males of all species observed except the raccoon dog dismounted from the female after intromission. The raccoon dog female lay on her side and back and the male.remained mounted on her. It is reported that the maned wolf also does not dismount from the female (Scherpner, pers. comm.). It is not known whether these differences are individual or species-specific. Cade, 967, and Cunningham (905) reported that the Cape hunting dog does not tie during copulation, a fact which points to a basic difference between the hunting dog and the remainder of the Family. Agonistic behavior. The complexity of social organization in each species in the Canidae is generally reflected in the postures and facial expressions assumed during agonistic encounters. Species with a highly developed social life such as the wolf and bush dog possess more specialized behavior patterns for expressing dominant and subordinate status and active agonistic behaviors such as attack, defense, flight, and submission. Since the emphasis will be on the most interesting species-specific differences in agonistic behavior, only a general description of postures and behavior patterns common to most members of the family will be presented. All of the postures and expressions used in expressing dominance and during a selfassured attack produce the impression of greater body size. The body is held rigid, the tail hair is raised, and the ears are erect with their openings pointed forward. Important species-specific differences are found in the tail postures of animals expressing their dominance. In the wolf, coyote, jackals, Paraguayan fox, and bush dog, the tail is held in a straight line extending the line of the back. The curled tail of the dingo, New Guinea singing dog, and domestic dog is a modification of this posture. The maned wolf raises its tail in a J-shape similar to that of the domestic dog, but there is evidence to suggest that the derivation of the two postures is different. Although presumably not closely related to each other, the raccoon dog and bat-eared fox possess a tail posture peculiar to themselves, an inverted U-shape observed in the expression of dominance, during attack, and also during sexual arousal in the males. In the red and Arctic foxes there is less difference between the animal expressing dominance and the normal unaroused animal. The visual effect of the erection of tail hair and the raised tail is enhanced in most Downloaded from on 07 June 08

5 SOCIAL BEHAVIOR IN THE CANIDAE 69 species by special tail markings. For example, raccoon dogs and bat-eared foxes have a black stripe extending along the length of the tail which becomes conspicuous with the tail in the inverted-u posture. The side-striped and black-backed jackals have similar black stripes, and the wolf, coyote, and Paraguayan fox possess black dots halfway down the tail and on the tail tip. Not surprisingly, the red and Arctic foxes, using less differentiated tail postures and movements, have less distinct markings. The self-assured attacking animal usually sinks his head, moves his ears so that the openings are pointed sideways, and whips his tail from side-to-side at a low frequency and a high amplitude. In the red and Arctic foxes, tail-waving is infrequent, but when it occurs it is closely associated with pawing movements of the fore and hind feet. The pre-attack posture of the bush dog does not include tail-waving, nor is it found in the raccoon dog and bat-eared fox who both raise their tail in the inverted U- shape previously described. (The bat-eared fox does show a slightly modified version of the pre-attack tail-waving pattern during play.) In the wolf, coyote, dingo, and New Guinea singing dog, a highly aroused dominant animal, or an animal about to attack, opens its mouth and bares its teeth by wrinkling the muzzle vertically. This is also said to occur in the golden jackal (Seitz, 959). This expression is a specialization of the above animals and has not been observed in other members of the Family. Most species only show a slight opening of the mouth before an attack. The corners of the mouth are pulled forward and create a short mouth crevice in self-assured animals of all species observed. In the members of most species there is no fixed sequence of events during a fight. Attack behaviors, such as stalking, chasing, body-slamming (slamming the hindquarters into the head or side of the opponent), and biting with head-shaking, alternate with one another and are found throughout the Family. More ritualized attack behavior is found in the bush dog where neck-biting and head-shaking take precedence over other behaviors. A subordinate animal may show behavior of flight, defense, and submission. In all of these cases, the posture and behavior create the illusion that the animal is smaller than he actually is. There is no erection of hair, the body is usually partially or completely lowered to the ground, and the tail is either wrapped around the hindquarters or tucked between the legs. A subordinate animal with little fear of being attacked wags its tail tip from side-toside at a high frequency and low amplitude, the anal region remaining covered by the upper part of the tail. Tail-wagging by a submissive individual occurs in all species except the raccoon dog. It is found less frequently in the red and Arctic foxes. Subordinate individuals are often observed seeking out the dominant animal in this crouching, tail-wagging posture and then either licking the dominant's lips or prodding the mouth corners of the dominant with the muzzle. If the dominant animal is asserting his authority, the subordinate may lie on his side or back, totally immobile, with the dominant standing over him. In the face of an animal demonstrating submission, the ears are spread at the base and the openings are pointed downward, the lips cover the teeth, and the corners of the mouth are pulled tightly back. In most species, a white area surrounding the mouth contrasts strikingly with the black lips and increases the visual impact of the submissive "grin." In the bush dog where there are no contrasting facial markings, the submissive "grin" has been exaggerated so that the mouth corners are opened and expose the molars. If the response to an aggressive opponent is neither submission nor total withdrawal, but defense, the defensive animal must actively prevent injury to itself by threat and/ or partial withdrawal. The body is usually lowered partly to the ground. In the foxlike species, back-arching is found where the head is sunk, the muzzle pointed upwards, and the back arched. The tail always covers the anus in a defensive animal, Downloaded from on 07 June 08

6 70 DEVRA G. KLEUMAN and there is rarely any movement of the tail. In the defensive threat, the ears are plastered back against the head. The wolf, coyote, dingo, and New Guinea singing dog bare the teeth, open the mouth slightly, and hold the corners of the mouth tightly back. In the remainder of the Family, the mouth is opened in a gape with the lips covering the teeth. Defensive, snapping, biting movements which are directed towards the opponent, but in space, are associated with defensive behavior in all species. DISCUSSION The members of most species in the Canidae are solitary and socialize with conspecifics primarily during the breeding season. These species possess uncomplicated means of communication and rely heavily upon sound and smell for information about conspecifics. During the evolution of the whole group, certain species have turned to groupliving. In the wolf, Cape hunting dog, and dhole, communal living is probably closely related to and has evolved with the hunting of large game. The reasons why a species such as the bat-eared fox is so gregarious are less obvious, but will probably be related ultimately to some aspect of this species' ecology. In the change from a solitary to a communal existence, there has occurred an elaboration of the "primitive" social behaviors which are found in a more solitary species such as the red fox. A constant association with conspecifics requires a more complex system of communication which could serve to reduce disruptive intraspecific aggression, and this has been fulfilled in the social species by a development of visual signals and other social behaviors. The pathways followed in this specialization of social behavior differ from species to species. Some species have exploited the use of visual signals more than others. The wolf, for example, now depends upon having a stable social hierarchy and some division of labor in order to maintain a workable hunting group. The order of rank is developed and maintained by behavior patterns which act as visual signals for conspecifics and reliably indicate the mood and social status of the individual. Two important areas of the body have been involved in the specialization of visual signals, the face and the hindquarters (Schenkel, 947). In the face, the gape threat which is found in the majority of the Family has been complicated by the introduction of teethbaring. This pattern also occurs in the coyote, domestic dog, and golden jackal. It indicates that the individual is highly aroused and very likely to attack. Dominant animals expose their teeth and open their mouth slightly while maintaining a short mouth crevice. A defensive individual also bares its teeth, but its mouth is opened wider and the corners of the mouth are pulled tightly back. Using these complex facial expressions, very slight differences of meaning can be conveyed to conspecifics. Neither the bush dog nor the Cape hunting dog appears to use the gape threat of the majority of the Family nor the teethbaring threat. In the bush dog, the submissive "grin" has been exaggerated, but the Cape hunting dog does not appear to have developed its facial expressions to any degree. In the wolf and many other species, the "primitive" tail-waving movements of the red fox have become specialized so that there now exist subtle differences in meaning determined by the frequency and amplitude of the side-to-side movements and up-and-down positions of the tail. The most-specialized tail postures can be seen in the wolf, coyote, domestic dog, side-striped and black-backed jackals, and the Paraguayan fox. The bush dog and Cape hunting dog show tail-wagging and up-and-down tail-positioning, but in a less complex manner than the other species. The raccoon dog and bat-eared fox possess the inverted-u posture which is unknown in the remainder of the family. This specific differentiation of the tailmovements and also of the tail-markings is undoubtedly related to the fact that the hindquarters are a significant center of olfactory stimuli. There are two important glandular areas in this region, the paired Downloaded from on 07 June 08

7 SOCIAL BEHAVIOR IN THE CANIDAE 7 anal glands and the gland located on the dorsal surface of the tail. These glands have been shown to exist in the majority of the Family (Hildebrand, 95). Almost certainly, the glandular secretions are used in conjunction with tail postures in communicating with conspecifics during social interactions. Along with the development of the visual signals associated with the maintenance of a social hierarchy, there has been a development in some species of other social behaviors. The raccoon dog and bat-eared fox possess a social hierarchy, in captivity at least, and possibly in the wild. Related to this, they have developed contact behaviors such as social grooming. Not all group-living species rely upon the social hierarchy to maintain group-cohesion. Kiihme observed no order of rank in the Cape hunting dog and believes that intraspecific aggression is channeled into the communal feeding ritual. During the feed, all individuals show submission towards one another by using postures derived from infantile begging. Kiihme observed no dominance interactions, and the author has observed no facial expressions for communicating threat or dominance in the hunting dog. At present, the classification of the Canidae is based upon anatomical differences, and especially upon differences in dentition. The bush dog, dhole, and Cape hunting dog have been placed together in one subfamily, the Simocyoninae, and the bateared fox is in a subfamily on its own, the Otocyoninae. The remaining species are all grouped together as the Caninae. The use of behavioral criteria for determining phylogenetic relationships between several members of the Family Canidae has not been attempted previously. On the basis of this preliminary study, certain tentative comments can be made about the way in which some of the species fall into groups. These groupings are based mainly upon the fact that certain species employ the same motor patterns in similar situations. In some cases there are discrepancies between the groupings which will be presented and the existing organization of the Family, but generally it has been found that those species which are considered to be closely related anatomically have strong behavioral affinities. The differences that do exist indicate that the positions of certain species ought to be re-evaluated, but sufficient data are not yet available to make more definite suggestions for a reorganization. The wolf, coyote, and domestic dog fall naturally into one group. Closely related to them, but separated on the basis of the teeth-baring pattern, are the black-backed and side-striped jackals. The Paraguayan fox has most in common with the two species of jackals and seems as unrelated to the fox-like members of the Family as the jackals are. Both anatomical and behavioral data indicate a close relationship between the red and Arctic foxes although the Arctic fox tends to be the more specialized animal. The members of both genera are separated from the wolves and jackals on the basis of many behavioral patterns. A possible relative of the foxes is the maned wolf, but we still have insufficient information on this animal. There are several very striking similarities between the raccoon dog and bat-eared fox which have been mentioned- So far as we know, these postures do not occur in other members of the Family. This suggests a close relationship between these two species which is rather surprising, considering their present positions in two separate subfamilies. The separation of the bush dog and Cape hunting dog (in the Simocyoninae) from the Caninae was not, in fact, confirmed by behavioral observations. Although both species utilize patterns which are found rarely or not at all in the remainder of the Family, they have very few patterns in common and are probably as widely separated from each other as they are from each member of the Caninae. A field study of the bush dog similar to Kiihme's excellent study of the Cape hunting dog would certainly clarify the positions of these two species. Downloaded from on 07 June 08

8 7 DEVRA G. KLEIMAN ACKNOWLEDGMENTS This research was supported by N.I.M.H. Grant MY-06. The author is deeply indebted to B. Ginsburg and D. Morris for their advice and encouragement throughout this research project and to G. H. Manley for his helpful criticisms of the manuscript. REFERENCES Cabrera, A., and J. Yepes Historia Natural Ediar. Mamiferos Sudamericanos. st ed. Compania Argentina de Editores, Buenos Aires, p Cade, C. E Intern. Zoo Yearbook 7:7-7. Cunningham, D. J Cape hunting dogs (Lycaon pieties) in the gardens of the Royal Zoological Society of Ireland. Proc. Roy. Soc. Edinburgh 5: Hildebrand, M. 95. The integument in Canidae. J. Mammal. : Krieg, W Im Lande des Mahnenwolfes. Zool. Gart. Leipzig : Kuhme, W Freilandstudien zur Soziologie des Hyanenhundes (Lycaon pictus lupinus Thomas, 90). Z. Tierpsychol. : Marlow, B. J. 96. Dingos. Australian Mus. Mag. 4:6-6. Mech, D. 96. Exit timber wolf, enter coyote. Animal Kingdom 64:89-9. Morris, D The mammals. Hodder and Stoughton, London, p. 48. Novikov, G. A Fauna of the U.S.S.R., Carnivorous mammals. Zool. Inst. Acad. Sci. U.S.S.R., no. 6 (Israel Program for Scientific Translations, Jerusalem, 96), p ; Ognev, S. I. 9. Mammals of Eastern Europe and Northern Asia, Vol. II. Carnivora (Israel Program for Scientific Translations, Jerusalem, 96), p Schenkel, R Ausdrucks-Studien an Wolfen. Behaviour :8-9. Schmidt-Nielsen, K Desert animals. Clarendon Press, Oxford, p Seitz, A Beobachtungen an handaufgezogenen Goldschakalen (Cam's aureus algirensis Wagner, 84). Z. Tierpsychol. 6: Sosnovskii, I. P. Intern. Zoo Yearbook 7:0-. Tembrock, G Zur Ethologie des Rotfuchses (Vulpes vulpes L.) unter besonderer Beriicksichtigung der Fortpflanzung. Zool. Garten, Leipzig :89-5. Van der Merwe, N. J. 95. The jackal. Fauna and Flora 4:-8. Young, S. P., and E. A. Goldman The wolves of North America. Am. Wildl. Inst., Washington, D. C. 66 p. (See p. 0-5). Young, S. P., and H. H. T. Jackson. 95. The clever coyote. Wildl. Mgt. Inst., Washington, D. C. p Downloaded from on 07 June 08