Behav Genet (2011) 41:803–809
DOI 10.1007/s10519-011-9459-0
ORIGINAL RESEARCH
Canid Mating Systems, Social Behavior, Parental Care
and Ontogeny: Are they Flexible?
Devra G. Kleiman
Received: 10 February 2011 / Accepted: 18 February 2011 / Published online: 13 April 2011
Ó Springer Science+Business Media, LLC 2011
Abstract Benson Ginsburg’s early studies of canid
socialization and wolf social and reproductive behavior were
focused, in part, on the degree to which there was flexibility
in social development and specifically whether there was a
critical period during development after which wolf pups
could not be socialized to humans. My focus was the degree
to which differences in canid ecology and social structure
were correlated with differences in the plasticity of social
and reproductive behavior, including development. Canid
species are unusual among the Mammalia in being primarily
monogamous. Males may play an indirect or direct role in
parental care, depending on a species degree of sociality.
Canid species also differ in developmental parameters, and
reproductive suppression is common in the group-living
pack hunters. I review comparative studies of the social and
reproductive behavior of three South American canids which
vary in their degree of sociality and explore the degree to
which the species are ecologically and socially flexible.
Keywords Monogamy
Behavioral plasticity
Canids

Sociality
Reproductive behavior
Edited by Stephen Maxson. Correspondence to: Department of
Psychology, University of Connecticut, Stoors, CT 06269-1020,
USA. email: Stephen.Maxson@UConn.Edu.
The paper originated in a festschrift, Nurturing the Genome, to honor
Benson E. Ginsburg on June 2, 2002 and is part of a special issue of
Behavior Genetics based on that festschrift. Devra G. Klieman passed
away in 2010, and her paper is published posthumously.
D. G. Kleiman
Division of Conservation and Science, Smithsonian National
Zoological Park, Washington, DC 20008, USA
Introduction
My interest in comparative behavior and the behavioral
flexibility of canids originated from two studies in which I
participated as an undergraduate at the University of Chi-
cago during the early 1960s. In both cases, my involvement
was due to Benson Ginsburg. First, Ginsburg was devel-
oping techniques to socialize wild wolves (Canis lupus)
and coyotes (Canis latrans) of different ages in order to
determine whether these social mammals pass through
critical periods during behavioral development that
restricts their ability to develop social bonds with humans
as adults (Ginsburg et al. 1962; Woolpy and Ginsburg
1967). As part of these studies, we used tranquilizers and
habituation to humans to bring about the development of
human-wolf bonds.
Second, I participated in annual observations of the
breeding activity of a wolf pack housed at Brookfield Zoo
in Chicago, overseen by George Rabb. The individual
behavioral differences and differing social relationships
within and between the sexes were especially interesting to
me (Rabb et al. 1967) and provided a window on the nat-
ural behavior of wolves that could be contrasted with the
behavior of the laboratory wolves.
From these experiences, I gained a unique knowledge of
canid social and reproductive behavior and social organi-
zation. Moreover, I had in-depth exposure to the nature-
nurture issue during the 1960s as seen in the differing
approaches to animal behavior from comparative and
physiological psychology and ethology. These undergrad-
uate experiences informed nearly all of my later research as
well as being so compelling that they derailed me from
pursuing a career in medicine. I had been planning to
become a psychiatrist. Through my career, I have main-
tained a fascination with individual behavioral plasticity
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and how the internal and external environment and phy-
logeny affect social relationships and social behavior.
Benson Ginsburg then provided me with an extraordi-
nary opportunity. I was looking for more background and
experience in classical ethology and to pursue studies of
canids. At an Ethological Conference at The Hague in
1963, Ginsburg met Desmond Morris, then Curator of
Mammals at the Zoological Society of London (ZSL).
Morris, an ethologist and former student of Oxford Uni-
versity’s Niko Tinbergen, mentioned that the ZSL had been
collecting specimens of numerous canid species and that he
was looking for someone to study them. Through his
National Institutes of Health grant, Ginsburg was able to
support me for a year’s research in London, the purpose of
which was to do comparative observations of canid social
behavior and to pursue studies of socialization, using spe-
cies other than wolves and coyotes.
I went to London for a year and remained for 5 years,
during which I conducted studies on the social and repro-
ductive behavior of numerous mammals and completed a
PhD in zoology through University College, University of
London. After a year doing canid research, I was hired by
the ZSL Wellcome Institute of Comparative Physiology as
a research assistant to do comparative behavior studies for
a World Health Organization (WHO)-funded program
investigating physiological delaying mechanisms in mam-
malian reproduction, including species with delayed fer-
tilization (insectivorous bats), delayed implantation
(mustelids) and prolonged pregnancies (South American
caviomorph rodents). One result was the first successful
captive reproduction of hibernating insectivorous bats
(Racey and Kleiman 1970).
My thesis was an in depth study of reproductive and
social behavior of a single rodent species, the green
acouchi, Myoprocta pratti (Kleiman 1969), and while
descriptive, the focus was on proximate causes of behavior.
My early studies of wolf social behavior and exposure to
physiological psychology had driven my interest in moti-
vation and hormone-behavior interactions. The ethological
influence in London added an evolutionary focus. Thus, I
included a comparative component in all of my work and
studied several other South American caviomorph rodents.
The variety of individuals and species of mammals that I
observed at ZSL had another result. I gained confidence in
my ability to distinguish between species characteristics
and an individual idiosyncrasy, e.g. I was the first to
describe the bizarre handstand urination and scent-marking
posture of the female bush dog (Speothos venaticus),
despite only having observed a single female in London
(Kleiman 1967, 1972).
Pursuing my interests in hormone-behavior interactions
and proximate mechanisms, I returned to the Institute of
Animal Behavior, Rutgers University, in 1969 on an
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National Institute of Mental Health (NIMH) Post-doctoral
Fellowship to investigate the hormonal influences under-
lying sex differences in the development of social behavior.
For the first time in my career, I worked with a laboratory
animal, the rat. But my interests in comparative behavior
and exotic animals drew me back to a zoo setting. In 1972,
I became the first woman scientist hired at the Smithso-
nian’s National Zoological Park.
Zoo research is restricted since the animal you are
studying is typically isolated from those critical environ-
mental characteristics in which it evolved. Thus, some
behavior patterns like predation may never be observed.
Additionally, stereotypies and abnormal behaviors may be
common in individuals who have had limited exposure to
natural environments, both social and asocial (Carlstead
1996).
But zoo research also has extraordinary benefits. Ani-
mals can be observed closely, and over long time periods,
even those that are not normally visible in nature. The
social environment and enclosure characteristics can be
manipulated and responses quantified. Many species can be
observed at once, thus providing a comparative perspective
(Kleiman 1992).
Over the course of my career, I have seen extraordinary
progress in zoo husbandry aided both by the explosion in
knowledge of the behavioral ecology of wild mammals and
of research on captive animals. Enclosures for captive
mammals have changed from the bare concrete-floored
cages of the 1950s and 1960s to enclosures which simulate
a natural habitat. The corresponding improvement in the
social and reproductive management of exotic mammals
has been informed by their species-specific needs and
behavior.
Monogamy
In the mid-1970s, I realized that several of the mammal
species with which I had worked exhibited monogamy as a
mating strategy (i.e. a single male and single female mated
exclusively with each other over multiple reproductive
cycles) and that they had several life history characteristics
in common, which differed from the typical polygynous
mammal (Kleiman 1977, 1981). For example, they showed
less sexual dimorphism than typically polygynous mam-
mals and fathers tended to exhibit paternal care. There also
seemed to be a continuum in the expression of monogamy,
depending on how social a species was (see Fig. 1). The
canids were a perfect subject of study since the taxon was
almost exclusively monogamous, yet species varied in the
level of sociality they exhibited. Wolves, African wild dogs
(Lycaon pictus), dholes (Cuon alpinus) and bush dogs
existed in large packs, hunted cooperatively, and had
Behav Genet (2011) 41:803–809
Solitary Pair Family Pack
& Sub-adults,
Juveniles Juveniles,
Infants
ASOCIAL SOCIAL
Fig. 1 Group size and social organization of mammalian species
exhibiting monogamy, depending upon the degree of sociality
(adapted from Kleiman, 1977)
complex social relationships. Less social species were
typically pair-bonded and lived as a pair outside of
breeding season; during rearing of the litter, they could be
seen as a nuclear family (Kleiman and Eisenberg 1973).
I developed a series of predictions concerning the life
history characteristics of monogamous mammals in general
and the variation likely to be observed, depending upon the
degree of sociality. With support from the Smithsonian
Institution and the NIMH, I then focused on testing these
predictions with students and colleagues, using the solitary
rufous elephant shrew (Elephantulus rufescens), the group-
living golden lion tamarin (Leontopithecus rosalia), and
three South American canid species that ranged from being
solitary to highly social.
The rufous elephant shrew, a small African insectivore,
is typically seen as a solitary individual in the wild.
Although a reproductive pair occupies a single territory, the
pair members rarely interact with one another. They have
small litters (usually 2) of highly precocial young, which
are ‘‘parked’’ in a safe site, with the mother and father
visiting separately and at infrequent intervals during the
day (Koontz 1984; Koontz and Roeper 1983; Rathbun
1979).
The golden lion tamarin, a territorial frugivorous-
insectivorous primate from Brazil’s Atlantic Forest, is
typically observed in groups of 4–6 individuals. The family
group includes the mated pair, twin or singleton infants,
and juveniles and sub-adults of varying ages; non-repro-
ductive adults are occasionally found within groups (Baker
et al. 2002). Golden lion tamarins have a mating system
and social structure much like wolves.
The three canid species, from the least to the most
social, were the maned wolf, crab-eating fox, and bush dog.
Maned wolves (Chrysocyon brachyurus) are tall thin fox-
like canids primarily from the grasslands of Brazil and
Argentina. They feed on small vertebrates and fruits. Adult
males and females are typically seen as solitary individuals
(Dietz 1984). Crab-eating foxes (Cerdocyon thous) are
805
medium-sized canids, wide-ranging throughout South
America, and feeding on small vertebrates, invertebrates,
insects and fruits (Brady 1981). Bush dogs are short stocky
canids. They are little-known, but may be seen in groups
and are known to prey as a pack on vertebrates larger than
themselves, e.g. pacas (Agouti paca).
For all five of the species, there were field as well as
captive observations supporting the hypothesis that
monogamy was the mating strategy, regardless of the
degree of sociality.
The focus of the captive canid studies was a comparison
of:
1. The degree of pair bonding behavior exhibited through
an examination of the quality and quantity of affilia-
tive, aggressive and sexual behaviors.
2. Parental care patterns, including the quantity and
quality of indirect and direct care behaviors, and the
quality and quantity of the contribution by adult
breeding males, adult breeding females and non-
breeding adults and sub-adults.
3. Ontogenetic patterns, including play and the develop-
ment of socio-sexual and feeding behavior.
4. Sex differences in behavior and reproduction, for
example, the degree and type of reproductive suppres-
sion exhibited by maturing sub-adults, the degree of
inter-sexual versus intra-sexual aggression and domi-
nance, and the degree of sexual dimorphism in
territorial behaviors such as scent-marking.
5. Species differences in the lability of these behaviors, if
that information could be obtained.
Over the period 1975 through the mid-1980s, the canids
were bred and observed at the Smithsonian National Zoo-
logical Park’s Conservation and Research Center.
Researchers, focusing on different questions, included
Chuck Brady, Ingrid Porton, Melissa Ditton Rodden,
Maxine Biben, James Dietz and the author (Biben 1982a, b,
c, 1983; Brady 1978, 1979, 1981; Brady and Ditton 1979;
Dietz 1984; Kleiman 1980, 1981, 1984; Kleiman and
Brady 1978; Kleiman and Malcolm 1981; Porton 1983;
Porton et al. 1987; Rodden et al. 1996; Biben et al.
unpublished observations). During the remainder of this
paper, I will not refer to individual publications, except
when I feel that the results need to be specifically cited.
Pair-bonding behaviors
The three South American canid species differed markedly
in many measures of social behavior that we predicted
would vary with the degree of sociality. For example, when
pairs are first introduced, male maned wolves may be very
aggressive towards females. Once paired, maned wolves
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exhibit more agonistic and defensive rather than affiliative
behaviors with each other, and they rarely interact or have
physical contact, e.g. they typically do not sleep together.
Indeed, they often carry out their asynchronous activities at
a considerable distance.
Crab-eating fox pairs, on the other hand, remain close
together much of the time and are more synchronous in
their activities although they hunt separately. They exhibit
sequence urine-marking regularly (Brady 1978) and exhibit
both defensive and affiliative behaviors in their social
interactions. Although aggressive at first introduction
(Biben 1982c), bush dog pairs eventually remain close to
each other, often sleeping in physical contact, and fre-
quently interact with affiliative/submissive behaviors. Bush
dog pairs also maintain contact using a high-pitched con-
tact call (Brady 1981), go into simultaneous submissive
behaviors (rolling on their sides) and may urine mark over
each other, the female using the unique handstand posture
that I first observed in the London Zoo (Kleiman 1972;
Porton 1983). They also exhibit almost completely syn-
chronous activity, including sequence urine-marking
(Porton 1983).
While both sexes may exhibit territorial behaviors such
as scent marking and long distance calling, social com-
munication behaviors in maned wolves are geared towards
a more solitary existence when compared with crab-eating
foxes and bush dogs. For example, maned wolves have a
deep-throated bark designed to carry over long distances
while bush dogs and crab-eating foxes often exhibit syn-
chronous urine marking and bush dogs vocalize
simultaneously.
Parental care behaviors
Kleiman and Malcolm (1981) divided mammalian parental
care behaviors into two types, INDIRECT CARE which
does not require physical contact between the adult and
young, and DIRECT CARE, which does require physical
contact. INDIRECT CARE behaviors include all the
activities involved in territorial acquisition, maintenance
and defense, which provide offspring with a protected
territory in which to grow. Specific behavior patterns which
may be expressed include inter-individual and inter-group
aggressive behavior towards conspecifics that intrude into
the territorial integrity of a pair or group. Long distance
vocalizations (e.g. wolf howls) and scent marking with
urine or glandular secretions on the borders of territories
may repel potential intruders.
Other INDIRECT CARE behaviors are shelter or den
construction, sentinel and anti-predator behaviors, and
caring for the pregnant mate through guarding and feeding
her. Except for the latter, both sexes and non-reproductive
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‘‘helpers’’ can and do perform all of these behaviors
although the existence of helpers and paternal care is rel-
atively rare among the mammals as a whole (Kleiman and
Malcolm 1981). There are, of course, species-specific dif-
ferences in which of these activities are expressed. For
example, the elephant-shrew is a cursorial mammal that
does not use shelters, dens or burrows, thus shelter con-
struction and maintenance is not in its repertoire of
INDIRECT CARE behaviors. INDIRECT CARE behav-
iors do not require physical contact with young, and since
many are necessary for individual survival and fitness, it
may be difficult to measure what portion might be con-
sidered relevant to individual fitness versus reproductive
success through survival of offspring and kin.
Patterns of DIRECT CARE include sleeping and resting
with young (which may contribute to thermoregulation of
altricial infants), grooming and cleaning young, retrieving
young, carrying or transporting young (more typical of
primates), babysitting for the young while the mother is
absent, feeding the young with regurgitated meat or small
prey carried directly back to the den, active defense of the
young against other larger carnivores and aggressive con-
specifics, and playing and socializing with young (see
Kleiman and Malcolm 1981).
Among the three South American canid species, the
timing, quality and quantity of male care varied depending
upon the degree of sociality (see Table 1 for canid parental
care behaviors). Maned wolf males generally exhibit more
indirect than direct parental care behaviors, especially
during the early part of the rearing period. Female maned
wolves may become aggressive towards the male after
giving birth and may prevent the male from entering the
den. Indeed, some pairs of captive maned wolves need to
be separated around the time of parturition. Yet, males
separated from the mate but still in close proximity may
respond to the female’s birth by exhibiting an increase in
territorial and ‘‘protective’’ behaviors, e.g. they may
become quite aggressive to their human caretakers
(Rodden, personal communication). However, once the
Table 1 Patterns of indirect and direct parental care in canids
(excluding nursing)
INDIRECT CARE DIRECT CARE
Resource acquisition Huddle with young
Resource maintenance Groom and clean young
Resource defense Retrieve young to den
Den construction Babysit
Sentinel and anti-predator behavior Play with young
Care of (feed) pregnant and/or Active defense of young
lactating female
Carry or regurgitate food to
young
Behav Genet (2011) 41:803–809
litter emerges from the den, male maned wolves may carry
food, regurgitate to the young and will interact and play
with young.
Male crab-eating foxes become involved with the litter a
little before den emergence since the female pair mate is
usually less aggressive at and shortly after parturition. Males
may enter the den in the female’s absence although they
usually rest and sleep at the entrance. They may also carry
food to the female and litter, which is left outside the den
entrance. Once the cubs emerge, the male participates
equally, retrieving and grooming young. In the wild, pairs
and their young travel together as a nuclear family unit for
about 5 months, at which time young disperse (Brady 1979).
The bush dog father’s parental care behavior is possibly
the most complex of any canid. Males are with the female
during parturition and help remove the young from the
birth canal as well as licking and grooming them. Males
may also remove and eat the placenta. The bush dog female
produces a very unusual high-pitched scream during the
birth process, which seems to attract the male (Porton,
personal communication). After the birth, the male remains
in close contact with the female and litter and basically
does everything the female does, except for lactating.
Female bush dogs may be unable to rear young in the
absence of the male (Jantschke 1973).
For all three canid species, the father interacts more with
the young than the mother, once the litter emerges from the
den. Young also show more submissive behavior to the
father and fathers seem to maintain subordination behavior
within the litter (Biben 1983). This is especially true for
bush dogs.
Social development
Maned wolf litters (*3 young) tend to be smaller than
crab-eating fox or bush dog litters (*5 young) (Moehlman
1997). Very early physical development tends to be similar
in all three species as well as the time course of the
development of social interactions, except that crab-eating
foxes develop more quickly (see Biben 1983). Maned wolf
pups spend the least amount of time in social interactions
and bush dogs the most, with peaks occurring between
weeks 12 and 18 in all three species. This corresponds to
the degree of sociality as adults in the three species.
In none of the species are clear dominance relations
developed during social interactions and play that persist
beyond the moment (Biben 1983). This contrasts with
observations that suggest that early fights and dominance
interactions have a profound effect on later social relations
(Bekoff 1978).
One of the more unusual findings was the difference in
the structure of play in the three species (Biben 1983).
807
Although bush dogs play more, both maned wolves and
crab-eating foxes have a more complex play behavioral
repertoire than bush dogs. Bush dog object play has few
elements and is characterized by group activity, e.g. 3 or
more pups might jointly carry and bite a wooden branch.
Social play is often initiated by submissive behaviors.
By contrast, crab-eating foxes and maned wolf object
and social play contains more behavior elements, is less
rigid and deterministic in structure and social play is more
dominated by ‘‘Play fighting’’, with many aggressive-
defensive behaviors. Object play is much more competitive
than in bush dogs.
The simplicity of bush dog play is surprising in view of
the prevailing belief that species which are more social will
have more complex social relationships as adults and more
complex play repertoires as juveniles. In fact, the differ-
ences in the complexity of object and social play in the
three species may derive from foraging and feeding dif-
ferences rather differences in the degree of sociality (Biben
1983). Both crab-eating foxes and maned wolves feed on a
variety of small to medium-sized vertebrates and inverte-
brates as well as fruits. They thus have relatively complex
foraging and feeding behaviors that may change seasonally
and in different habitats (see Brady 1978). Play may
function more to develop the flexibility that is needed to
exploit multiple changing food sources.
Bush dogs, by contrast, appear to be almost exclusively
pack hunters who bring their large prey (pacas and capyb-
aras, Hydrochaeris hydrochaeris)) down as a group simply
by biting it until it drops. The hunting tactics are therefore
simple. It is important, however, that bush dogs be non-
competitive while hunting, and their object and social play
does reinforce submissive and cooperative behaviors.
Reproductive development and suppression
Maned wolves breed once yearly and young disperse prior
to the next breeding season. Crab-eating foxes may breed
twice yearly and thus litter dispersal likely occurs within
the first 6 months. For both species, sexual maturity and
breeding occurs at the earliest opportunity. Bush dog
females may also exhibit multiple reproductive cycles
during the year, especially if a litter is lost, but until young
females are removed from their natal group, they will not
exhibit an estrous cycle. Indeed, unlike most canids, young
bush dog females can be brought into heat within weeks by
exposing them to an unfamiliar male (Porton et al. 1987).
Thus, bush dogs exhibit the same suite of characteristics
seen in other canid pack hunters with obligate monogamy:
hunting large prey, living in complex social groups, large
litters, extensive direct paternal care and adult reproduc-
tively-suppressed helpers (Moehlman 1997).
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Discussion and conclusions
The three South American canid species are all monoga-
mous in mating strategy, but differ in their degree of
sociality. This diversity more than likely derives from
ecological differences, specifically species’ variation in
feeding habits, with maned wolves and crab-eating foxes
feeding on a variety of fruits, small vertebrates, and
invertebrates (including insects and crabs) that require
variation and flexibility in foraging strategies. Bush dogs,
however, are more strictly carnivorous, being pack hunters
like wolves and African wild dogs and bringing down prey
larger than themselves. Their group hunting strategy, while
obligate, may be much simpler and more stereotyped than
the foraging behavior of the other two species.
Social differences are reflected in many aspects of the
three species’ life history characteristics from the quality
and quantity of pair-bonding behaviors, to the timing, type
and amount of paternal behavior, the degree of involve-
ment in parental care by non-reproductive adult helpers,
social development and play, and both hormonal and
behavioral reproductive suppression (Moehlman 1997).
The degree to which either social or ecological charac-
teristics are flexible and whether there is a correlation
between the degree of sociality, complexity of social
interactions, ability to form a human-canid bond and for-
aging strategy, is unclear. Certainly, some species like
coyotes are enormously flexible in their ecological
requirements and feeding behavior. Their prey base varies
tremendously; they may feed on fruits, small vertebrates,
insects, invertebrates, carrion, or hunt down small ungu-
lates. Correlated with this is considerable variation in group
size and social structure (Kleiman and Brady 1978).
Additionally coyotes are persecuted by humans. Thus
they may survive as solitary individuals, or in a pair,
nuclear family or a pack. Their adaptability to human-
induced environmental disturbance and to persecution has
actually resulted in a huge expansion of their range and
distribution, just in our lifetimes (Kleiman and Brady
1978). The ecological and social adaptability of coyotes,
however, has not translated into a tendency for them to
form bonds with humans or to be tamed. Indeed, they are
present in many urban and suburban U.S. settings, but
remain shy and quite distant from people.
Bush dogs require social interactions and do not thrive
when maintained as solitary individuals. They do easily
become tame and indeed were often maintained by South
American Native Americans as pets. But their social
behavior is not that complex, being focused on submissive
behaviors.
Both maned wolves and crab-eating foxes can be
habituated (tamed) to humans, but certainly maned wolves
are often best maintained in situations where they are not
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constantly in forced close contact with a conspecific (even
a pair-mate) or humans. Indeed, within the zoo community,
they are most often described as shy and sensitive to human
disturbance. Maned wolves may show the most individual
variability in social and parental behaviors, as described in
the zoo literature, but it is difficult to separate this vari-
ability from known variability in zoo husbandry and
management. Ultimately, it is not clear to what degree
intra-specific social bonding tendencies can be extrapolated
to the human-canid social bond.
The basic common characteristic for the three South
American species is bonding with a single member of the
opposite sex, but the greater sociality of some species in this
group, e.g. bush dogs, may not necessarily derive from a need
for greater complexity of social relations. Bush dogs appear
able to hunt cooperatively simply by being non-competitive
and maintaining complex submissive behaviors among pack
members. Thus, their play and social ontogeny is consider-
ably simpler and more rigid than for the other species.
Interestingly, in this respect they are more similar to African
wild dogs than to wolves. The latter has a more variable diet
and foraging strategy over a wide part of its range, its group
size varies significantly with diet, and social structure is
generally conceded to be complex.
Acknowledgments I would like to thank Benson Ginsburg for
giving me a start in canid research and supporting my interests so
completely. Without the opportunities he provided, my career would
have gone in a very different direction. I also wish to thank George
and Mary Rabb for introducing me to the complexities of life within a
wolf pack. I would also like to thank those colleagues that contributed
so much to the canid studies, especially: Maxeen Biben, Chuck
Brady, James Dietz, John Eisenberg, Ingrid Porton, and Melissa
Rodden. These studies were supported by grants from the Smithso-
nian Research Foundation and NIMH 27241-03.
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