Carnivores and Behaviour:
Compiled as a final-year zoology student at the University of Edinburgh, based on the information given in lectures.
History and phylogeny of Carnivora
Defined nowadays as the
descendants of a common ancestor, rather than on the basis of shared
Carnivore body plan is typical
of a quadrupedal mammal - no significant lengthening of limbs or loss of
Carnivora vary enormously in
size - the Kodiak bear is 10,000 times the size of the least weasel.
Carnivora arose in Laurasia
(the northern continents) and radiated to other parts of the world (Martin
Not all members of order
Carnivora are flesh-eaters (e.g. panda eats bamboo, kinkajou eats flowers and
Pinnipeds (seals and sea lions)
are now considered monophyletic, due to similarity in flipper structure (Wyss 1988) and molecular evidence.
Phylogenetic trees can be
combined using a 'super matrix' of the characters used in different trees
(though this is likely to be full of holes) or a 'super-tree' based upon the
conclusions of each tree. Newer and more reliable studies should perhaps be
weighted more highly when constructing super-trees. (Sanderson et al 1998)
Phylogeny of carnivores
(based on MacDonald
/ /------------------- Ursidae
/ / /- Otariidae
/--CANIFORMIA-< / /-<
| (Canoidea) \--ARCTOIDEA--< /--PINNIPEDIA-< \- Odobaenidae [?]
| \-< \
| \ \--- Phocidae
| \ /------- Procyonidae
| \ /
CARNIVORA \-----< /-- Mephitidae
| \-- Mustelidae
| /----------- Felidae
| / \----------- Hyaenidae
(Feloidea) \ /--------- Viverridae
Canidae (dogs) - built for cursorial
hunting and long-distance chases; can regurgitate food for young.
Mustelidae (weasels etc) - have long,
thin bodies for getting into small spaces.
Mephitidae (skunks) - a New World family
that deter predators with noxious compounds.
Ursidae (bears) - are omnivorous (have
chewing teeth rather than carnassials), lack whiskers, hibernate in northern
areas, and can live off fat reserves in extreme environments. Includes giant
Procyonidae (raccoons) - mostly
insectivorous and New World. May include red panda (Slattery & O'Brien
Viverridae (civets) - molecular evidence
suggests that this 'family' is paraphyletic (Yoder et al 2003).
Herpestidae (mongooses) - includes
Hyaenidae (hyenas) - includes the
Felidae (cats) - obligate flesh-eaters
with reduced dentition (hardly any molars); hunt by stealth.
Phocidae (true seals) paddle with back
flippers and steer with front ones.
Otariidae (eared seals - fur seals and
sea lions) propel themselves in the water with forelimbs, and can pull hind
limbs under body for use on land.
Odobenidae (walrus) combines features of
Harris 1991, The handbook of British
mammals; Macdonald & Barrett 1993, Mammals
of Britain and Europe; Yalden 1999, The history of British mammals)
Fox, Vulpes vulpes - Urban foxes are a
potential rabies vector, if the disease ever returns to Britain.
Wolf, Canis lupus - extinct since 18th century.
Pine marten, Martes martes - has elongated
legs; hunts in trees for birds and red squirrels. Restricted to Scotland -
could be reintroduced to England, but conflicts with bird conservation.
Stoat, Mustela erminea, and weasel, Mustela nivalis - long slender bodies, short legs; hunt down burrows. Weasel is
highly sexually dimorphic - driven by sexual selection (facilitating polygyny)
and environmental selection (males and females specialise in different prey).
Female stoats are mated during infancy - allows early reproduction and
successful colonisation. (Macdonald 2000)
Polecat, Mustela putorius - mainly
restricted to Wales, but recently spread back into England. Hybridisation with
feral ferrets is a problem.
Feral ferret, Mustela furo - introduced 1100.
Originated from M. putorius
or Steppe polecat M. eversmanni.
Mink, Mustela vison - elongated body; a
vicious predator of birds and small mammals. Released from fur farms. Doesn't
compete with otter (separate niches); might compete with polecat but currently
living in separate areas.
Badger, Meles meles - legally protected. May
act as a vector for TB in cattle.
Otter, Lutra lutra - population
recovering after being badly affected by river pollution.
Wildcat, Felis silvestris - Hybridisation
with domestic cat is a big problem. It is difficult to define a
"wildcat". There is no baseline data on DNA. True wildcats have heavy
tails with thick black tips and broad striping; skeletons differ from that of
domestic cat. Wildcats are legally protected but feral tabby cats (which look
Feral cat, Felis catus - introduced.
Lynx, Lynx lynx - extinct since early postglacial period.
Brown bear, Ursus arctos - extinct by 10th
Harbour (common) seal, Phoca vitulina - widely
distributed in north Atlantic and north Pacific.
Grey seal, Halichoerus grypus - exists as four
separate populations in north Atlantic.
Both species are sedentary
Occasional visitors to British
waters: bearded seal, hooded seal, walrus.
Grey seal pups have white,
non-insulating fur. Harbour seal pups, by contrast, can swim from birth - they
are typically born in summer when water is warmer.
Male harbour seals attempt to
defend aquatic territory around pupping sites. There is low variance in male
reproductive success, and no mate fidelity (number of full sibs no greater than
predicted by random model).
During breeding seasons, male
harbour seals balance competing demands of foraging (most intense during
pre-mating period) and encountering females (there is weight loss during mating
period due to less foraging).
Male grey seals defend females,
not territory. They fast for up to six weeks (they are bigger than harbour
seals, with more endurance). There is evidence for polygyny (degree may depend
upon topography and ease of female defence), and mate fidelity (both through
site preference and partner preference).
Mother grey seals fast during
lactation. Mother harbour seals are smaller and don't have sufficient body
resources to fast for the whole lactation period (Coltman
et al 1997).
Jaws and dentition
& Van Valkenburgh 1996, in Carnivore behaviour, ecology and evolution)
Long canine teeth are used to
deliver a stabbing/suffocating bite.
Blade-like carnassial teeth
(upper 4th premolar and lower 1st molar) are used for
Canoids use post-carnassial
teeth for crushing bone; feloids lack molars and use pre-carnassial teeth for
Long canines of sabre-toothed cats
(e.g. Smilodon) would have been
vulnerable to breakage if stabbed deep into prey; sabretooths probably killed
with sabre slashes and incisor battery.
Carnivores typically have large
temporalis, pterygoid and digastricus muscles (involved in opening/closing
jaws), but small masseter muscles (involved in chewing).
Meat eaters (e.g. lion: I 3/3, C 1/1, PM
3/2, M 1/1) - stabbing canines and incisors, powerful carnassials with blade
parallel to jaw for maximum strength, cheek teeth well-adapted for grinding
bones and chewing flesh.
Insectivores (e.g. aardwolf: I 3/3, C
1/1, PM 3/1-2, M 1/1-2) - canines reduced and incisor-like, carnassials less
prominent with blade at an angle to jaw, cheek teeth not adapted for grinding,
teeth generally weak and small.
Omnivores (e.g. brown bear: I 3/3, C
1/1, PM 4/4, M 2/3) - incisors moderately sized with less need for tearing
flesh, long canines for stabbing and killing small prey, reduced carnassials,
large and versatile molars for grinding.
Fish eaters (e.g. harbour seal: I 3/2, C
1/1, post-canines 5/5) - definite incisors and canines for killing bites,
conical post-canines adapted for chewing fish rather than crushing bones, fewer
incisors, no carnassials.
(Davies 1991, in the book Behavioural Ecology)
Types of mating system:
monogamy, polygyny, polyandry, promiscuity (indiscriminate mating)
Females should invest in
obtaining resources; males should invest in obtaining mates.
Female dispersion should be
influenced by resources; male dispersion should be influenced by female
Mammals (unlike birds) should
be polygynous or promiscuous, unless there is a need for paternal care.
Factors affecting mating
systems: dispersion, economics of female defence by males, need for paternal
care, phylogenetic inertia, life history (K-selected or r-selected), ecological
factors promoting group formation, habitat constraints, reproductive
specialisations, outbreeding mechanisms.
In lion and hyena groups (as in
most mammals), males emigrate. In African hunting dog packs, females emigrate.
In most fissipeds, litter size
depends on conditions. Pinnipeds, by contrast, almost always have one pup at a
In solitary carnivores, female
range depends on food abundance, especially at the most critical time of year.
Small, exclusive ranges are
expected when food resources are stable and evenly-distributed; large,
overlapping ranges are expected when there is spatial and temporal variation in
Male spatial organisation
should be related to food resources outside the breeding season, and to female
distribution during the breeding season. Male ranges are larger than predicted
on the basis of food requirements, overlapping many female ranges (Sandell 1989, in Carnivore
behaviour, ecology and evolution).
In pinnipeds, ecological
factors facilitate and constrain polygyny, and hence sexual dimorphism.
Parturition occurs on land, is highly seasonal and synchronised (with an annual
cycle, except in walrus), males are attracted to parturition sites for access
to females, and there is no paternal care of young.
Most pinnipeds breeding on land
(e.g. sea lions, elephant seals) or on land-fast ice (e.g. Weddell seal, ringed
seal), where suitable sites are stable but not abundant, are polygynous (due to
crowding) and spend longer periods on shore. There is more polygyny in the
Antarctic, in the absence of land predators (polar bears).
Pinnipeds breeding on pack ice
(e.g. hooded seal), which is unstable but abundant,
show increased synchrony, shorter time on substrate, and less polygyny. (Exception:
walrus is a polygynous ice-breeder, perhaps partly due to phylogenetic inertia.)
Land-breeding harbour seal populations form larger groups and are more sexually
dimorphic than ice-breeding populations, suggesting greater polygyny. (Le Bouef 1986, in New
Sexual behaviour and reproduction
An animal's reproductive
strategy is linked to its life history. Covarying factors include: longevity,
size, number of litters, litter size, growth rates, and investment in
There is a continuum of
life-histories between small, short-lived animals with frequent, large litters,
and large, long-lived animals with infrequent small litters.
Stoats have an annual breeding
cycle, whereas weasels may have two litters in good years (Macdonald 2000).
Births are timed to maximise
survival of offspring; this affects the timing of mating.
Number of young reared depends
on female's condition. In some species litter size is linked to prey abundance
- spotted hyenas' conception rates are lowest at times of year when prey is
least abundant (Holekamp et al 1999).
Embryonic diapause (delayed
implantation) occurs in polar bears and various mustelids and pinnipeds. It
appears to have evolved once in the common ancestor of these groups, but has
been secondarily lost in some species.
Delayed implantation in some
mammals (e.g. kangaroos) is facultative - it occurs during the period of
lactation, with female 'constantly pregnant' - but in carnivores it is
obligatory. (Mead 1993)
Delayed implantation dissociates
mating and reproduction, and allows mating to be done at a convenient time. It
has fitness costs (loss of fecundity), especially in warmer climates and in
smaller species. In mustelids, delayed implantation occurs in bigger species
and colder climates (Thom et al 2004), e.g. in stoat but not in weasel.
'guarantees pregnancy' - it is valuable when it is vital to give birth early,
and allows subordinates in a group to hedge their bets. It is useful in
In stoats, embryos implant in
spring in response to increasing photoperiod (Macdonald 2000); in badgers (in
which gestation period is longer), embryos implant in autumn in response to
Polar bear embryos are
implanted in autumn; tiny cubs are born and suckled in mid-winter while mother
is hibernating and emerge in spring (Pond 1989).
In pinnipeds, delayed
implantation allows birth and mating to be done at the same time (so animals
only risk coming ashore once), while maintaining an annual cycle.
Female spotted hyenas have
'false penises', which make mating and birth awkward and dangerous. Why incur
this handicap? Hyena societies are very competitive, with strong selection for
female aggressiveness, which has been achieved through androgenisation. False
penises are used in social displays. (Frank 1997)
(Stoddart 1976, Mammalian odours and pheromones)
Rate of urine marking in the
vixen is highest: during the breeding season, on frequently-used paths, on
outbound journeys, and near core of animal's range. Vixens often explore and
re-mark previously-marked patches (overmarking). When markings from strangers
are artificially placed within a vixen's range, she will investigate
thoroughly, appear disturbed, and re-mark the spot. (Macdonald 1979)
Marking with faeces by badgers
is done at shared latrines along territorial boundaries, and at unshared
latrines in territory's 'hinterland'. Boundary latrines are used most
frequently during the breeding season, and are mainly used by males (Roper et
Spotted hyenas living in poorer
areas with larger ranges mark the hinterland, whereas those in smaller ranges
mark the boundaries - economics of defence.
There is a trade off between
longevity and volatility of odour molecules.
Mammals, unlike insects, often
use heavy, waxy secretions containing complex mixtures of compounds.
Hyenas can produce two types of
anal gland secretion: a short-lived watery one and a long-lived waxy one.
Pheromones, defined as a
specific molecule eliciting a specific response, are probably rare in mammals.
Odour-detecting membranes are
on endoturbinales deep within nose. Dogs do a series of little sniffs to force
air into sinuses that contain a lot of their olfactory epithelium. They exhale
sideways to avoid re-breathing stale air.
Skin secretions come from
sebaceous glands, apocrine glands (sweat glands associated with hair follicle)
and eccrine glands (sweat glands not associated with hair follicles).
Sebaceous glands produce oily,
long-lasting secretions, under the control of steroid hormones.
Apocrine and eccrine glands
produce watery short-lived secretions under nervous/blood hormone control.
Other sources of odour: saliva,
accessory gland at corner of eye, urine, vaginal secretions.
Animals may mark conspicuous
landmarks, mark social companions (allomarking), or release odours into the
Functions of social odours:
identity, reproduction and detection of oestrus, temporal information ("I
was here"), territory and social status. (Gorman & Trowbridge 1989, in
Carnivore behaviour, ecology and
Possible reasons for scent
marking territories (Gosling 1982): deterring intruders, intimidating
intruders, enhancing confidence of resident, informing intruders about status
of the resident, orientating the resident, attracting or stimulating mates,
assisting pair-bond formation, assisting population regulation, assisting
optimal foraging, associating the resident with its territory (an intruder is
unlikely to attack the resident, who will fight hard).
Living in groups is not the
norm in carnivores: only 10-15% of fissiped species do so outside the breeding
Two main benefits of group
living: assistance in killing large prey, and defence.
Additional advantages of groups
- defending prey, social learning, locating unpredictable prey, division of
labour, alloparental behaviour (babysitting), sexual competition, territory
There is a positive
relationship between group size and territory size in some species (coyotes,
wolves, lions, spotted hyenas), but not in others (badgers, red foxes). Why?
Resource dispersion hypothesis - animals choose minimum territory needed to
support themselves, and if food is patchy a territory
sufficient for some may accommodate others too. Prey renewal hypothesis - when
prey is rapidly-renewing there is plenty to go round.
Babysitting in meerkats (Clutton-Brock et al 1998) - some (usually subordinates)
guard burrow while others forage. Babysitters incur a cost - lost foraging
opportunity. In larger groups, each individual spends less time babysitting.
Small carnivore species tend to
be solitary, perhaps because they eat small food items that are difficult to
share. (Exception: one group of related herpestids, in which group living has evolved.)
Medium-to-large species are
likely to be solitary if they hunt small, indivisible prey (e.g. foxes, maned
wolf) or if they hunt by surprising prey in low-visibility habitats (e.g.
Phylogenetic constraints may
also play a part: felids tend to be solitary, while canids are more social.
Larger hunting groups take
larger prey (e.g. in lions, hyenas, wolves) but each individual doesn't
necessarily get a bigger portion. There is an optimum pack size that maximises
an individual's food intake.
Success rate in hunting may
also be important (e.g. jackals can only steal gazelle fawns by working in
Larger canids live in larger
groups. Larger groups take proportionately larger prey. Diet breadth increases
with body size in co-operative hunters, but is independent of body size in
solitary hunters. (Moehlman & Hofer 1997)
In lions, co-operative hunting
may only occur at times of scarcity or when tackling huge prey (though plenty
of solitary cat species also tackle prey much bigger than themselves). Food
intake per lion per day is highest when alone or in groups of 5 to 7. Lions may
forage in non-optimal group sizes because of constraints imposed by protection
of cubs (in crèches), territorial defence, and the risk of meeting larger
groups (Packer et al 1990).
Reproductive success amongst a
'coalition' of male lions is less skewed when they are brothers.
In hunting dogs, modal pack
size appears to optimise food intake per dog per kilometre chased, but
variation in data is enormous, and the measure of cost may be wrong (benefit
minus cost should be measured instead).
Jackals live in monogamous
families with helpers. The number of helpers correlates with the number of
young reared, but we shouldn't assume causation. Manipulation experiments are
difficult to do on carnivores.
Byers 1998, Animal play: evolutionary,
comparative and ecological perspectives)
'Play' is easy to recognise but
hard to define.
Play often includes repetitive
or exaggerated actions, sudden switches in behaviour, and/or self-handicap.
Play is a characteristic of
more intelligent animals (certain mammals and birds).
Rats play more obviously than
mice do - does this reflect larger brain size?
Types of play: locomotor play,
social play, object play (latter is usually the last to emerge).
Function of play (Smith 1982):
Physical training? Building competitive social skills (fighting)? Building
non-competitive social skills (social bonding, acquisition of rank,
communication)? Building cognitive skills?
Male offspring typically
play-fight more than females, but this may because they get less attention from
Play incurs costs: time and
energy, risk of injury, risk of predation due to lack
of vigilance. For example, in young fur seals play occupies only 6% of the
time, but 80% of deaths due to predators occur during play (Harcourt 1991).
Artificial experiments into
play are hard to do because it is difficult to stop animals playing without
restricting them in other ways. However, natural experiments exist. Lee (1994)
observed no difference between monkeys that grew up under easy conditions and
played a lot, and those that grew up under harsh conditions and played less.
Kittens weaned earlier play
precociously, suggesting that play is important (Bateson
et al 1990).
Play may be important for
synaptogenesis - the development and refinement of neural connections (Furlow 2001).
Play may facilitate the
development of 'coping strategies' for dealing with situations (Spinka et al 2001).
Y = b(Ma)
where M is body mass, Y is another measurement, a (exponent of allometry) and b
(coefficient of allometry) are constants. Parameters estimated from straight
line: log Y = a(log M) + log b. (Huxley 1972)
In positive allometry, a >
1; in negative allometry, a < 1; in isometry, a = 1.
For carnivore skull mass or
brain mass vs. body mass, a < 1. For heart mass vs. body mass, a = ~1.
For mammal skeleton mass vs.
body mass, a > 1, due to a heavier body's greater need for support.
Development of behaviour - the mother-offspring
Young may be altricial (highly
dependent on mother at birth) or precocial (born at a more advanced stage).
Milk is thicker and fattier in
pinnipeds than in fissipeds, although between pinnipeds there are differences,
depending on maternal strategy (Oftedal 1984).
In domestic cat, adult males
are larger than females, but males' growth spurt occurs late in development, so
the rearing of sons is not significantly more strenuous for a mother than the
rearing of daughters.
There is a conflict of interest
between youngsters and their siblings (e.g. competition for nipples to suckle).
There is also a conflict
between the offspring (which want a greater share of the mother's resources)
and the mother (who wants to maximise her overall lifetime reproductive
Lactation can be a very costly
process (much more costly than gestation), especially for larger mammals.
Mothers typically gain weight
during pregnancy and lose it during lactation (exception: the dwarf mongoose,
which loses weight during pregnancy, perhaps due to a trade-off between
carrying weight and greater mobility).
In badgers, body condition
scarcely deteriorates after undergoing pregnancy without lactation, but
deteriorates dramatically after pregnancy and lactation (Woodroffe
& Macdonald 1995).
Energy intake of mother cat
increases by 100-200% at the time of peak milk yield, but she still loses
Gut length may increase during
lactation (e.g. in rats) to meet the demands of greater food intake.
A mother cat with larger
litters produces more milk, but there is a limit to her capacity to do this, so
growth rate is faster among kittens in smaller litters (Deag
et al 2000).
Later in the lactation period,
mother cats increasing deny milk to kittens, by changes in posture (e.g. use of
'blocking posture'), or in lab experiments by retreating to a shelf that
kittens can't reach.
As lactation progresses,
feedings are increasingly initiated by kittens rather than by mother.
Weaning is a process during
which there is a sharp drop in rate of parental investment in offspring (Martin
Growth curves of offspring kink
upwards at the time of weaning (especially in bigger litters), since growth is
no longer constrained by the mother's capacity for milk production. Weaning is
inevitable since there comes a point at which milk can no longer satisfy the
youngsters' increasing energy requirements.
The role of conflict in weaning
may have been overstated - it is not in young carnivores' interests to exhaust
their mother completely during lactation because she still has to bring back
solid food and teach them to hunt.
Mothers bring back dead prey at
first, then start to bring back live prey for kittens
to practice with. Later on, kittens begin to participate in the hunt for
Kittens' play becomes increasingly
associated with predatory behaviour as they grow older (Caro
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