Crucial importance of pack size in the African wild dog Lycaon pictus
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Animal Conservation (2001) 4, 169–174 © 2001 The Zoological Society of London Printed in the United Kingdom
Crucial importance of pack size in the African wild
dog Lycaon pictus
Franck Courchamp1 and David W. Macdonald2
1
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
2
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK
(Received 22 May 2000; accepted 18 December 2000)
Abstract
Although the massive organized slaughter of African wild dogs, Lycaon pictus, largely ended several
decades ago, this endangered canid continues to decline and faces extinction. Several lines of evi-
dence suggest that this arises from obligate cooperative breeding, which makes Lycaon more sensi-
tive to anthropogenic mortality. A number of behaviours in this species are characterized by a reliance
on helpers. These include cooperative hunting, defence from kleptoparasitism, pup feeding and baby-
sitting. As a result, there are strong, positive relationships between pack size and the production and
survival of pups, and pairs of wild dogs are often unsuccessful at raising offspring without the assis-
tance of helpers. Consequently, a pack in which membership drops below a critical size may be caught
in a positive feedback loop: poor reproduction and low survival further reduce pack size, culminat-
ing in failure of the whole pack. Here, we review the literature to reveal the importance of pack size
in the African wild dog. Most importantly, we argue that there is a critical minimum threshold, below
which packs face an increasing probability of extinction – an Allee effect with consequences for the
conservation of this species, and of other obligate cooperators.
INTRODUCTION population dynamics and thereby to explain an impor-
tant element of their current decline.
African wild dogs, Lycaon pictus, also called painted
It has been hypothesized that, because of their need
hunting dogs (Rasmussen, 1999), have been consistently
for helpers, obligate cooperative breeders require a min-
persecuted by human populations throughout known his-
imum size to persist as a group (Courchamp, Grenfell
tory (Estes & Goddard, 1967). Although the govern-
& Clutton-Brock, 1999b; Courchamp, Clutton-Brock &
ment-funded slaughter ended a few decades ago,
Grenfell, 2000). Theoretically, below this critical thresh-
anthropogenic mortality is still the main factor of
old, a social group that suffers what is called ‘inverse
African wild dog mortality (Fuller et al., 1992;
density dependence’ because of a lack of helpers will
Fanshawe et al., 1997). Remaining wild dog populations
have a reduced survival and/or breeding success, which
have shown dramatic decreases over the past 30 years,
will further decrease its size, ultimately drawing it to
resulting in their disappearance from 25 of the 39 coun-
extirpation. This is one form of Allee effect, an inverse
tries in which they were formerly recorded (Fanshawe
density dependence at low density or population size,
et al., 1997). This has left the entire species with a much
typically below a threshold (Courchamp, Clutton-Brock
reduced geographical distribution and a small number of
& Grenfell, 1999b; Stephens & Sutherland, 1999). Our
packs (600–1000, Fanshawe et al., 1997). Since most of
purpose here is to review the literature to reveal the
the remaining populations number less than 100 indi-
importance of pack size for African wild dogs.
viduals, it is predicted that, if nothing is done, extinc-
tion of the species could occur in the short term
(Woodroffe & Ginsberg, 1997a). Averting this disaster Importance of pack size
requires understanding the causal mechanisms of the
African wild dogs live in packs of up to 20 adults and
continuous decline of these populations. Here we focus
their dependent young (Childes, 1988; Fuller et al.,
on just one characteristic of the population dynamics of
1992; Maddock & Mills, 1994; Creel & Creel, 1995).
wild dogs, and attempt to link individual behaviour to
Generally, only the alpha pair breeds, assisted by sev-
All correspondence to: F. Courchamp, Ecologie, Systématique et
eral helpers who generally do not breed themselves. In
Evolution, Batiment 362, Université Paris Sud, 91405 Orsay Cedex, Table 1 we summarize representative illustrations of the
France. Tel: (0033/0) 16915 5685; Fax: (0033/0) 16915 5696; need for helpers in Lycaon for three aspects of their fit-
E-mail: franck.courchamp@epc.u-psud.fr ness: foraging, breeding and survival.170 F. COURCHAMP AND D. W. MACDONALD
Table 1. Mechanisms providing advantages to large packs in African wild dogs
Advantage of Process Examples of reference
large packs
Foraging Hunting efficiency
(lower energetic cost) Simultaneous attacks Fanshawe & FitzGibbon, 1993; Creel & Creel, 1995
Prey isolation Kühme, 1965; Creel & Creel, 1995
Distract mother from calf Fanshawe & FitzGibbon, 1993; Creel & Creel, 1995
Intercept prey after shortcut Kühme, 1965; Estes & Goddard, 1967; Creel & Creel, 1995
Shorter chases Creel & Creel, 1995
Simultaneous kills Creel & Creel, 1995
Prey species range Pull prey together to a halt Creel & Creel, 1995
Maintain/distract prey while Fanshawe & FitzGibbon, 1993; Creel & Creel, 1995
being disembowelled
Injury reduction Maintain head Creel & Creel, 1995
Prey killing Coordinated tearing apart Estes & Goddard, 1967; Carbone et al., 1997
Carcass eating Coordinated carcass opening Estes & Goddard, 1967; Rasmussen, unpublished data
and dismembering
Defense from Rapid carcass cleaning Estes & Goddard, 1967; Fanshawe & FitzGibbon, 1993;
kleptoparasites Rasmussen, unpublished data
Intimidation by numbers Malcolm & Marten, 1982; Fuller & Kat, 1990; Fanshawe &
FitzGibbon, 1993; McNutt, 1996a
Steals from Intimidation by numbers Creel & Creel, 1995
kleptoparasites
Breeding Litters size Prior access to kills to Malcolm & Marten, 1982
breeding female and juvenile
Pregnant/suckling female Malcolm & Marten, 1982
fed by regurgitation at the den
Pup care Facultative communal care Kühme, 1965; Fuller et al., 1992; Burrows, 1995
Pups fed by regurgitation
for 3 months Kühme, 1965; Malcolm, 1979; Malcolm & Marten, 1982
Parts of a kill carried to pups Malcolm & Marten, 1982
Pups led to kills Malcolm & Marten, 1982
Pups given priority at kills Malcolm & Marten, 1982
Survival Pup survival Baby-sitting (+ baby-sitter Kühme, 1965; Malcolm & Marten, 1982
fed by regurgitation)
Pup defence against Kühme, 1965; Malcolm & Marten, 1982; McNutt, 1996a
predators
Pup adoption McNutt, 1996a
Adult survival Injured and older dogs Estes & Goddard, 1967; Malcolm & Marten, 1982
tolerated at kills
Increased predator vigilance McNutt, 1996a
in large packs
Intraspecific Clashes between packs Creel & Creel, 1995, 1998
competition
Larger dispersing Lower mortality Creel & Creel, 1995
cohorts Possibility of pack takeover Creel & Creel, 1995; Creel et al., 1998
Better chances of successful
establishment of new pack Creel & Creel, 1995
Creel & Creel, 1995), hunting in larger packs extends
Foraging the range of prey species that a pack can hunt – an advan-
Lycaon helpers contribute to diverse aspects of foraging. tage when smaller prey are not available close to the den
Wild dogs are known to hunt cooperatively, typically in during the denning period (Fanshawe & Fitzgibbon,
packs of between seven and ten (Schaller, 1972; 1993). Therefore, not only does hunting success (per-
Fanshawe & Fitzgibbon, 1993; Fuller & Kat, 1993; Creel centage of kills per hunt) increase with pack size, but so
& Creel, 1995). There is evidence that several individ- does the mass of the prey killed, while the distance
uals hunt more efficiently than do pairs or singletons chased per hunt decreases with pack size (Creel & Creel,
(Fanshawe & Fitzgibbon, 1993; Creel & Creel, 1995). 1995).
Specifically, wild dogs cooperate to isolate prey, launch A second benefit of larger pack size to foraging for
simultaneous attacks, intercept fleeing animals after a Lycaon concerns defence of the kill from kleptopara-
shortcut, distract mother from calf, together pull a prey sites. Spotted hyaenas, Crocuta crocuta, and lions,
to a halt and restrain it while being killed (Creel & Creel, Panthera leo, regularly steal the kills of wild dogs
1995). Together with reducing the risks of injury from (Fanshawe & Fitzgibbon, 1993; McNutt, 1996a;
large or well-armed prey (Malcolm & Marten, 1982; Carbone, DuToit & Gordon, 1997; Gorman et al., 1998),Importance of pack size in wild dogs 171
sometimes even before the captured prey is killed (Estes to hunt is compromised in late pregnancy and early lac-
& Goddard, 1967; Creel & Creel, 1996). A small loss tation (Woodroffe & Ginsberg, 1997a). They also feed
of food to kleptoparasites may have a large impact on the pups for 2 to 3 months by regurgitating meat (Estes
the amount of time that dogs must hunt to achieve energy & Goddard, 1967; Malcolm & Marten, 1982), even if
balance (Gorman et al., 1998). Larger packs are able to the mother dies before their independence (Estes &
retain kills from hyaenas for longer (Malcolm & Marten, Goddard, 1967; McNutt, 1996a). Pack members also
1982; Fuller & Kat, 1990; Fanshawe & Fitzgibbon, give pups priority access to food, even when it is scarce,
1993; Creel & Creel, 1996; McNutt, 1996a; Carbone et although, when very hungry, juveniles may not regurgi-
al., 1997). Lycaon themselves engage in kleptopara- tate to the pups (Malcolm & Marten, 1982). As the pups
sitism and have been documented stealing the kills of mature, some adults may carry part of a kill to the pups
leopards, lions and hyaenas (Creel & Creel, 1995), and for them to chew (Malcolm & Marten, 1982). Later still,
it seems likely that larger packs would be at an advan- the pups follow the adults to the kill (or are led there by
tage in accomplishing such thefts. juveniles), where they will again have the possibility of
Lycaon kill their prey by tearing it apart, dogs grab- feeding first while the adults guard the carcass (Malcolm
bing it from all sides and pulling against one another & Marten, 1982; Rasmussen, 1997).
(Estes & Goddard, 1967; Carbone et al., 1997). This This helping behaviour may facilitate large litter sizes.
task, together with dismembering the carcass, is more Certainly, litter size is correlated with pack size
rapidly accomplished by many dogs than by few, (Vucetich & Creel, 1999). Although limited by small
decreasing the time for which the kill is available to klep- sample size (packs of five or less were rare and seldom
toparasites. Wild dog digestive tracts are exceptionally bred successfully), other published data are suggestive
adapted to allow rapid ingestion of large amounts of of this effect (Fuller et al., 1992).
meat, and to regurgitate these later on (Ewer, 1973: see
below). Each dog can carry 3 days’ worth of food, a full
Survival
stomach containing up to 4.4 kg of meat (Reich, 1981
in McNutt, 1996a), and possibly twice that amount A third point where the cooperative behaviour of wild
(Creel & Creel, 1995). Rapid consumption and success- dogs is of major importance concerns survival, for exam-
ful defence of a kill reduces the number of hunts nec- ple during interactions with natural enemies. Breeding
essary, and consequently their energetic cost (Gorman females can regain hunting condition 3 weeks after par-
et al., 1998) as well as the risks linked to the hunt (acci- turition. Her return to the hunt is important, especially
dent, predator encounter, death of the pups left behind, as alpha females often lead hunts (J. McNutt,
Malcolm & Marten, 1982; Creel & Creel, 1995). Smaller pers. comm.; G. Rasmussen, pers. comm.). However, lit-
packs are slower to dismember and eat carcasses, but ters cannot follow the pack for another 2 months. A
also may be unable to consume all the flesh and obliged baby-sitter may then be left with the pups while the rest
to leave food behind, thereby promoting the survival of of the pack is hunting. The baby-sitter must chase away
competitors. predators, make sure the pups do not stray, and warn
them to go down the den if danger threatens (Kühme,
1965; Malcolm & Marten, 1982). However, leaving a
Breeding
baby-sitter behind is costly for three reasons. First, this
Cooperation is crucial to Lycaon pup-rearing. Their lit- individual will have to be fed by meat regurgitated
ters are uniquely large amongst canids: averaging 10–11 from the hunting party, thereby diminishing the food
pups, maximum 21 pups (Fuller et al., 1992). In gen- available for the pups (Kühme, 1965; Malcolm &
eral, only the alpha female bears and nurses pups. When Marten, 1982). Second, the baby-sitter’s absence
a subordinate female breeds, the alpha may simply take lowers the hunting efficiency of the pack (which is
her pups and suckle alone the combined litters (Burrows, related to the number of hunters). Third, it also reduces
1995), but more commonly the females share the bur- by 4 kg or so the food brought back to the den (plus
den of suckling the two litters in a communal den that food then becomes available to competitors). In
(Kühme, 1965; Fuller et al., 1992; Burrows, 1995). In fact, the threshold pack size at which leaving baby-
addition to providing alternative rest periods to the two sitters on duty becomes generally economic seems
mothers (who may participate in hunts sooner, Malcolm to be around five individuals (Courchamp et al., in
& Marten, 1982), this may also have a survival value press).
for the two litters, since it may allow the transfer of more African wild dogs do not take risks to defend a car-
maternal antibodies to both of them (Roulin & Heeb, cass from lions or hyaenas, but will aggressively mob
1999). potential predators if these threaten the pups (e.g.
In the context of the Allee effect, a more important Kühme, 1965; Estes & Goddard, 1967). The ferocity and
aspect of cooperative breeding lies in Lycaon’s regurgi- organization of their defence can drive off spotted hyae-
tating behaviour. African wild dogs are able to ingest nas, jackals, leopards or even lions (Malcolm & Marten,
and then regurgitate large amounts of meat, on average 1982; Creel & Creel, 1995; McNutt, 1996a), an impor-
about 1 kg of meat after a full meal (Kühme, 1965; Ewer, tant cause of mortality in wild dogs (Mills & Gorman,
1973; Malcolm, 1979, in Fuller & Kat, 1990). In this 1997). Large packs are evidently more efficient at mob-
way, they may feed the pregnant mother, whose ability bing predators than are intermediate sized packs.172 F. COURCHAMP AND D. W. MACDONALD
In addition, incapacitated individuals (because of a Finally, because of a probable pack size threshold, the
debilitating disease or injury) are tolerated at kills by union of two small dispersal units (of one or two dogs)
other members of the pack even when they cannot par- is less likely to produce a successful new pack than if
ticipate in the hunt (Estes & Goddard, 1967), and may two larger units join. All this has been shown to occur
be fed by regurgitation (G. Rasmussen, unpublished with a theoretical model (Courchamp et al., 2000). This
data). Clearly, this is likely to enhance the chance of is supported by empirical data from Selous and
recovery and subsequent full participation in the pack. Serengeti, where pack extinction rates of 16% to 37%
Older members, less able to hunt, may none the less effi- per year have been recorded between 1985 and 1991
ciently chase predators from the dens, and regurgitate (Burrows, 1995; S. Creel, unpublished data, see also
generous amounts to the pups, and are tolerated at kills Ginsberg, Mace & Albon, 1995).
(Malcolm & Marten, 1982).
DISCUSSION
Consequences at the pack level: direct empirical
Our synthesis reveals many aspects of Lycaon behaviour
evidence
– including foraging, breeding and survival – for which
Although the weight of literature strongly suggests an a critical number of members is essential for the persis-
Allee effect in Lycaon, proof is elusive. Each of the three tence of packs and populations. It may be important to
fitness components reviewed above seems positively note that we do not imply that African wild dogs can-
linked with pack size, but none can be unequivocally not reproduce below this critical pack size: there are
proven individually. However, one of the most straight- some anecdotes of that. Our point is rather that statisti-
forward ways of evaluating the importance of pack size cally the break point between success and failure hov-
for wild dogs is to compare the number of pups suc- ers around a pack size of five adults.
cessfully raised to independence for different pack sizes. Our aim is to emphasize an additional force for the
Any such relationship can be attributed to a combina- extinction and decline of wild dogs throughout Africa
tion of an improved foraging efficiency, breeding suc- that aggravates disproportionately the widely acknowl-
cess and survivorship in larger packs. Analysis of edged dangers threatening this species. We argue that
empirical data showed in several studies that the num- the impacts of the probable causes of these population
ber of pups successfully raised increases with pack size declines – persecution, habitat destruction and natural
(Malcolm & Marten, 1982; Burrows, 1995; Creel, Creel enemies (predators, competitors and parasites) – are
& Monfort, 1998; G. Rasmussen, unpublished data). magnified by the very nature of the dynamics of oblig-
ate cooperative breeders. This concept has not been
advanced as a potential cause for high rate of pack
Consequences at the population level
extinction, although the importance of pack size has pre-
Intraspecific competition has been implicated as a major viously been emphasized by wild dog specialists (Estes
cause of adult and pup mortality (Creel & Creel, 1998). & Goddard, 1967; Malcolm & Marten, 1982; Fanshawe
An encounter between two packs may result in severe & Fitzgibbon, 1993; Fuller & Kat, 1993; Burrows, 1995;
fights leading to lethal injuries: in Selous, seven wild Creel & Creel, 1995; McNutt, 1996a; Carbone et al.,
dogs were killed in such inter-pack fights (Creel & Creel, 1997; Creel et al., 1998; Vucetich & Creel, 1999).
1998). In these clashes, the larger pack always took the Obviously, there will be upper limits to group size
advantage over the smaller one (ten cases, Creel & Creel, through intra-group competition, for feeding and for
1995). In absence of other selective pressure acting in breeding opportunities, and ultimately because of a
the opposite direction, this could be sufficient for a nat- diminished marginal advantage of expanded member-
ural selection towards larger groups to occur. ship (Macdonald & Carr, 1989). The existence of such
Wild dog pack dynamics are also influenced by dis- an optimum should be expressed as a dome-shaped dis-
persal of young adults. Generally, several males of the tribution of pack size, explicable if populations were
same cohort disperse together, and may join lone subject to an Allee effect: inverse density dependence at
females, or a cohort of females (Frame et al., 1979; low density and direct density dependence at high den-
Fuller et al., 1992; Burrows, 1995; McNutt, 1996b). sity (in this case it is pack size, rather than density, which
Mortality during dispersal is likely to be important, con- matters). This is exactly the type of distribution, with a
sidering the large distances and dangers involved. Large mode at ten dogs, observed in the largest existing pop-
packs are more likely to produce large sex-same dis- ulation of African wild dogs: Selous Game Reserve in
persal cohorts, which may lower the mortality during Tanzania (Creel, 1997). Literature data reanalysed by
dispersal (Frame et al., 1979; Creel & Creel, 1995). Fuller and co-authors (1992), as well as studies from
Smaller packs may not produce dispersers, or produce Childes (1988) and from Maddock & Mills (1994), con-
too small a cohort for it to survive long enough to estab- firm this average pack size at ten adults. Irrespective of
lish itself on an empty territory. In addition, the fewer the precise values or the minimum threshold and opti-
(and the smaller) the neighbouring packs, the less sin- mum pack size, it appears that these two crucial num-
gle-sex cohorts of the opposite sex are potentially avail- bers are not widely separate, which suggests that a
able, which may increase the time before mate location delicate balance exists, from which Lycaon may readily
and new pack establishment (Frame et al., 1979). be perturbed.Importance of pack size in wild dogs 173
From a conservation perspective, the existence of a Courchamp, F., Clutton-Brock, T. H. & Grenfell, B. T. (1999a).
critical pack size for wild dogs implies two different Inverse density dependence and the Allee effect. TREE 14:
options for wild dog conservation. Obviously, pack sizes 405–410.
Courchamp, F., Clutton-Brock, T. H. & Grenfell, B. T. (2000).
should not be eroded towards the critical threshold,
Multi-group dynamics and Allee effects in the African wild dog
which requires alleviating the major causes of individ- Lycaon pictus. Anim. Conserv. 3: 277–286.
ual mortality: persecution and human activities (e.g., Courchamp, F., Grenfell, B. T. & Clutton-Brock, T. H. (1999b).
snare poaching, road traffic and domestic dog induced Population dynamics of obligate cooperators. Proc. R. Soc.
epidemics) (Maddock & Mills, 1994; Woodroffe & Lond. B 266: 557–564.
Ginsberg, 1997a). Wild dog conservationists have long Courchamp, F., Rasmussen, G. S. A & Macdonald, D. W. (In
advocated such approaches. A less obvious line of press) Pack size imposes a trade-off between hunting and baby-
sitting in the painted hunting dog Lycaon pictus. Behav. Ecol.
thought would be to increase artificially the size of packs Creel, S. (1997). Cooperative hunting and group size: assump-
known to be at risk because of low numbers. While tions and currencies. Anim. Behav. 54: 1319–1324.
release of captive-bred Lycaon has proven problematic Creel, S. & Creel, N. M. (1995). Communal hunting and pack
(Scheepers & Venzke, 1995), wild dogs readily accept size in African wild dogs, Lycaon pictus. Anim. Behav. 50:
unrelated individuals, or even adopt unrelated pups or 1325–1339.
juveniles (McNutt, 1996a). In this regard, the fact that Creel, S. & Creel, N. M. (1996). Limitation of African wild dogs
all four documented cases of adoption of unrelated pups by competition with larger carnivores. Conserv. Biol. 10:
526–538.
came from ‘smaller-than-average groups’ (McNutt, Creel, S. & Creel, N. M. (1998). Six ecological factors that may
1996a) may be considered as a further indication that limit African wild dogs, Lycaon pictus. Anim. Conserv. 1: 1–9.
pack size per se is a major factor influencing wild dog Creel, S., Creel, N. M. & Monfort, S. L. (1998). Birth order, estro-
survival. Artificial constitution of packs in captivity also gens and sex-ratio adaptation in African wild dogs (Lycaon pic-
shows some promise (Rasmussen, 1997; Woodroffe & tus). Anim. Repr. Sc. 53: 315–320.
Ginsberg, 1997b; Woodroffe & Ginsberg, 1999). At the Estes, R. D. & Goddard, J. (1967). Prey selection and hunting
behaviour of the African wild dog. J. Wildl. Mgmt. 31: 52–70.
least, the concept of critical threshold should be consid-
Ewer, R. F. 1973. The carnivores. Ithaca, NY: Cornell University
ered when planning wild dog translocations. In this con- Press.
text, it is noteworthy that the number of packs is also of Fanshawe, J. H. & FitzGibbon, C. D. (1993). Factors influencing
critical importance for a closed population to persist the success of an African wild dog pack. Anim. Behav. 45:
(Courchamp et al., 2000). 479–490.
Our critical analysis of the literature has revealed Fanshawe, J. H., Ginsberg, J. R., Sicllero-Zubiri, C. & Woodroffe,
compelling evidence of a threatening Allee effect for R. (1997). The status and distribution of remaining wild dog
populations. In The African wild dog: status survey and con-
Lycaon. Other highly cooperative species are likely to servation action plan: 11–57. Woodroffe, R., Ginsberg, J. R.,
be equally susceptible to these processes, making it a Macdonald, D. W. & the IUCN/SSC Canid Specialist Group
priority to test empirically the largely theoretical evi- (Eds). Gland, Switzerland: IUCN.
dence that the operation of this process at the group level Frame, L. H., Malcolm, J. R., Frame, G. W. & van Lawick, H.
will create an additional Allee effect at the population (1979). Social organization of African wild dogs (Lycaon pic-
level. tus) on the Serengeti plains, Tanzania 1967–1978. Z.
Tierpsychol. 50: 225–249.
Fuller, T. K. & Kat, P. W. (1990). Movements, activity, and prey
Acknowledgements relationships of African wild dogs (Lycaon pictus) near Aitong,
southwestern Kenya. Afr. J. Ecol. 28: 330–350.
This work was supported by the Société de Secours de Fuller, T. K. & Kat, P. W. (1993). Hunting success of African
Amis de la Science. The authors wish to thank Tim wild dogs in southwestern Kenya. J. Mammal. 74: 464–467.
Clutton-Brock and Bryan Grenfell for inspiring discus- Fuller, T. K., Kat, P. W., Bulger, J. B., Maddock, A. H., Ginsberg,
sions about the likelihood of Allee effect in obligate J. R., Burrows, R., McNutt, J. W. & Mills, M. G. L. (1992).
Population dynamics of African wild dogs. In Wildlife 2001:
cooperative breeders and its modelling, respectively. We
populations. McCullough, D. R. & Barrett, R. H. (Eds). London:
are also grateful to them and to Greg Rasmussen, Scott Elsevier Applied Science.
Creel and Rhys Green for discussions and critical read- Ginsberg, J. R., Mace, G. M. & Albon, S. (1995). Local extinc-
ing of the manuscript. tion in a small and declining population – wild dogs in the
Serengeti. Proc. Roy. Soc. Lond. B 262: 221–228.
Gorman, M. L., Mills, M. G., Raath, J. P. & Speakman, J. R.
REFERENCES (1998). High hunting costs make African wild dogs vulnerable
to kleptoparasitism by hyaenas. Nature 391: 479–481.
Burrows, R. (1995). Demographic changes and social conse- Kühme, W. (1965). Communal food distribution and division of
quences in wild dogs, 1964–1992. In Serengeti II: dynamics, labour in African hunting dogs. Nature 205: 443–444.
management and conservation of an ecosystem: 385–400. Macdonald, D. W. & Carr, G. M. (1989). Food security and the
Sinclair, A. R. E. & Arcese, P. (Eds). Chicago: University of rewards of tolerance. In Comparative socioecology: the behav-
Chicago Press. ioural ecology of humans and other mammals: 75–99. Standen,
Carbone, C., DuToit, J. T. & Gordon, I. J. (1997). Feeding suc- V. & Folley, R. A. (Eds). Oxford: Blackwell Scientific
cess in African wild dogs: does kleptoparasitism by spotted hye- Publications.
nas influence hunting group size? J. Anim. Ecol. 66: 318–326. McNutt, J. W. (1996a). Adoption in African wild dogs, Lycaon
Childes, S. L. (1988). The past history, present status and distri- pictus. J. Zool. 240: 163–173.
bution of the hunting dog Lycaon pictus in Zimbabwe. Biol. McNutt, J. W. (1996b). Sex-biased dispersal in African wild dogs,
Conserv. 44: 301–316. Lycaon pictus. Anim. Behav. 52: 1067–1077.174 F. COURCHAMP AND D. W. MACDONALD Maddock, A. H. & Mills, M. G. L. (1994). Population character- Schaller, G. B. (1972). Serengeti lion: a study of predator–prey istics of African wild dogs Lycaon pictus in the eastern relations. Chicago: University of Chicago Press. Transvaal Lowveld, South-Africa, as revealed through photo- Scheepers, J. L. & Venzke, K. A. E. (1995). Attempts to reintro- graphic records. Biol. Conserv. 67: 57–62. duce African wild dogs Lycaon pictus into Etosha National Park, Malcolm, J. R. (1979). Social organisation and the communal Namibia. South Afr. J. Wildl. Res. 25: 138–140. rearing of pups in African wild dogs (Lycaon pictus). PhD the- Stephens, P. A. & Sutherland, W. J. (1999). The Allee effect and sis, Harvard University. its consequences for ecology and conservation. TREE 14: Malcolm, J. R. & Marten, K. (1982). Natural-selection and the 401–405. communal rearing of pups in African wild dogs (Lycaon pic- Vucetich, J. A. & Creel, S. (1999). Ecological interactions, social tus). Behav. Ecol. & Sociobiol. 10: 1–13. organization, and extinction risk in African wild dogs. Conserv. Mills, M. G. L & Gorman, M. L. (1997). Factors affecting the Biol. 13: 1172–1182. density and distribution of wild dogs in the Kruger National Woodroffe, R. & Ginsberg, J. R. (1997a). Past and future causes Park. Conserv. Biol. 11: 1397–1406. of wild dogs’ population decline. In The African wild dog: sta- Rasmussen, G. S. A. (1997). Conservation status of the painted tus survey and conservation action plan: 58–74. Woodroffe, R., hunting dog Lycaon pictus in Zimbabwe. Ministry of Environ- Ginsberg, J. R., Macdonald, D. W. & the IUCN/SSC Canid ment & Tourism, Department of National Parks & Wildlife Specialist Group (Eds). Gland, Switzerland: IUCN. Management, Zimbabwe. Woodroffe, R. & Ginsberg, J. R. (1997b). The rôle of captive Rasmussen, G. S. A. (1999). Livestock predation by the painted breeding and reintroduction in wild dog conservation. In The hunting dog Lycaon pictus in a cattle ranching region of African wild dog: status survey and conservation action plan: Zimbabwe: a case study. Biol. Conserv. 88: 133–139. 100–111. Woodroffe, R., Ginsberg, J. R., Macdonald, D. W. & Reich, A. (1981). The behaviour and ecology of the African wild the IUCN/SSC Canid Specialist Group (Eds). Gland, dog (Lycaon pictus) in the Kruger National Park. Ph. D., Yale Switzerland: IUCN. University. Woodroffe, R. & Ginsberg, J. R. (1999). Conserving the African Roulin, A. & Heeb, P. (1999). The immunological function of wild dog Lycaon pictus. I Diagnosing and treating causes of allosuckling. Ecol. Let. 2: 319–324. decline. Oryx 33: 132–142.
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