Behavioral Ecology Vol. 13 No. 1: 20-27
© 2002 International Society for Behavioral Ecology
Small pack size imposes a trade-off between hunting and pup-guarding in the painted hunting dog Lycaon pictus
a Large Animal Research Group, Department of Zoology, University of Cambridge, UK b Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, UK c Painted Hunting Dog Research Project, Natural History Museum, PO Box 240, Bulawayo, Zimbabwe
Address correspondence to F. Courchamp, who is now at Ecologie, Systématique & Evolution, Université Paris-Sud XI, Bâtiment 362, F-91405 Orsay Cedex, France. E-mail: franck.courchamp{at}epc.u-psud.fr .
Received 2 April 2000; revised 14 November 2000; accepted 4 February 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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The painted hunting dog or African wild dog, Lycaon pictus, is one of the most endangered large carnivores in Africa, with extinction predicted within a few decades if their dramatic decline is not stopped. It has recently been hypothesized that because of their constraining need for helpers, group size was of major importance in obligate cooperative breeding species, and that the resulting likely existence of a threshold number of adults could create an Allee effect, increasing the group extinction risk. One example where the importance for a critical number of adults may have major repercussions for painted hunting dogs concerns baby-sitting, or pup-guarding, a behavior typical of obligate cooperative breeders. We propose that, as forgoing this behavior is costly because pup guards have the potential to decrease pup mortality, its use is costly too, especially in small packs, because helpers are strongly needed for their cooperative foraging (hunting, protecting the kill and bringing back food to the pups). We present a simple model showing how pup-guarding imposes a cost because it implies that less food per hunt is brought back to more individuals at the den. We complete these analyses with empirical tests of the effect of pack size on the probability of pup-guarding, from field data from the Hwange population in Zimbabwe. Our model, as well as our 5 years of empirical data, both suggest a critical threshold at a size of about five individuals.
Key words: African wild dog conservation, Allee effect, cooperative hunting, inverse density dependence, Lycaon pictus, painted hunting dog, pup-guarding.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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The painted hunting dog, Lycaon pictus, often called the African wild dog (but see Rasmussen, 1999
) is among the most endangered large carnivores in Africa, and
most of the 600-1000 remaining packs are known to be in populations too small
to be viable (Woodroffe and Ginsberg,
1997). As a result, complete extinction of the species is
predicted imminently unless the precise causes for its decline are rapidly
understood and action taken to alleviate them
(Fanshawe et al., 1991;
Ginsberg and Macdonald, 1990).
Even though several causes of mortality in Lycaon are well documented
(see Creel and Creel, 1998;
Woodroffe and Ginsberg, 1999
for reviews), the precise mechanisms endangering this species in particular
have not yet been entirely elucidated. In particular, it might be wondered
whether natural processes alone (such as competition and predation) can really
explain why populations of Lycaon are declining more rapidly than
those of sympatric carnivores, which also suffered from persecution and
habitat fragmentation (Creel and Creel,
1998). Lycaon is an obligate cooperative breeder living
in packs of up to 20 adults, in which most of the time only the alpha pair
breeds; the remaining adults are reproductively suppressed and help to raise
the pups (Childes, 1988;
Creel and Creel, 1995;
Fuller et al., 1992;
Maddock and Mills, 1994).
Obligate cooperative breeders, such as Lycaon, have evolved to such a
point that their need for helpers may become a constraint
(Clutton-Brock et al., 1999;
Jennions and Macdonald, 1994).
For example, the need for a certain number of helpers to carry out several
behaviors essential to the group (including foraging, breeding and survival)
may result in a minimum group size, hence an Allee effect
(Courchamp et al., 1999;
Stephens and Sutherland,
1999). In other words, smaller groups would have increasing
difficulties to maintain themselves, to such a point that most packs under a
critical number of adults could often be led to extinction.
One advantage of cooperative breeding in Lycaon is that a pack
member can protect the pups during the months where they cannot follow the
hunting party, and it is on this particular aspect of breeding that this work
is focused. The common advantages of this behavior in Lycaon include:
watching pups to prevent loss, alerting them to danger (lions, Panthera
leo, or spotted hyaenas, Crocuta crocuta) thus ensuring they go
to the safety of the den, protecting them from smaller predators or
conspecifics, and moving them when heavy rain may cause floods at the den
(Malcolm and Marten, 1982).
Baby-sitting occurs both during the denning and pup caching periods, and both
periods are covered by our present data (see below). Evidence that the
presence of an adult at the den is beneficial for the pups in terms of
survival includes the study by Malcolm and Marten
(1982), which provided typical
examples of the protection against predators provided by the baby-sitter to
the pups. On several occasions, the baby-sitter either ran back to the natal
den or went back underground with the pups, or chased away predators close to
the den. That study also recorded nine cases where a dog returned to the den
to baby-sit after encountering a predator close by. In a similar vein, on one
occasion in this study, the presence of at least one lion caused a yearling
male baby-sitting 12 week old pups to move them a distance of 1.8 km away from
the danger. Other potential advantages of baby-sitting are that first the
mother, often an experienced hunter, may be allowed to go back sooner to hunt
if a subordinate dog guards the litter and second she is enabled to get back
into vital body condition post whelping so essential to the peripatetic life
style of this hypercursorial canid.
The main apparent disadvantage of baby-sitting is that the individual
assuming this task cannot participate in the hunts. Because Lycaon
hunt cooperatively, and its hunting success is related to the hunting party
size (Creel, 1997;
Creel and Creel, 1995), small
packs will tend to have a lower hunting efficiency than larger packs. Though a
single dog has been recorded to kill an adult kudu, Tragelaphus
strepsiceros, cow (this study), they will generally also be less likely
than larger packs to tackle large prey. Moreover, larger hunting parties are
less likely to lose kills to kleptoparasites because they reduce carcass
access time and the presence of a single individual may make a difference
(Carbone et al., 1997;
Creel and Creel, 1996;
Fanshawe and Fitzgibbon, 1993;
Gorman et al., 1998). Finally,
and most importantly here, adults regurgitate food back at the den for the
pups once they are able to eat solid food at the age of 2 to 3 weeks and
during the ensuing 2 to 3 months (Estes
and Goddard, 1967; Malcolm and
Marten, 1982; McNutt,
1996). Pups are dependent on regurgitation until they can follow
the hunting party and feed directly at the kill
(Malcolm and Marten, 1982;
Rasmussen, 1997). Leaving a
guard with the pups during hunts is thus energetically detrimental for three
reasons. First, the total amount of food regurgitated by the hunters will be
lower if one adult did not participate in hunts (and this may be exacerbated
by the lower hunting efficiency of smaller hunting parties). Second, the
individual guarding the pups, especially if it is the lactating mother, will
consume part of the meat regurgitated by the hunters
(Kühme,
1965; Malcolm and Marten,
1982), a part which will thus not be available to the pups. This
energetic disadvantage can be increased if more than one adult baby-sits, as
has sometimes been observed (Malcolm and
Marten, 1982). Third, reduced intakes will lead to supplementary
hunts which expose the pack to additional risks associated with hunting and
high energy expenditure (Gorman et al.,
1998).
This behavior is generally called baby-sitting when the pack member is a nonbreeding helper, but in our study we must consider all instances where a pack member was left with the pups (either the mother or a helper). In addition, when a pack member is left at the den, it is most often the alpha female (89.7% of the pup-guarding occurrence in our data set). For these reasons, we will from now on refer to "pup-guarding" rather than "baby-sitting."
Nonbreeders guard the young at the den in a variety of cooperative
carnivores (Solomon and French,
1996) and virtually all studies of vertebrates with such guarding
behavior show that removal of guards leads to a substantial reduction of
offspring (Clutton-Brock,
1991). As it is for the benefits, the presence of pup-guarding
cost seems widespread, although it may differ among species. For example in
suricates, Suricata suricatta, individuals forego foraging for the
duration of pup-guarding, which is very costly
(Clutton-Brock et al., 1998;
Doolan and Macdonald, 1999).
Although in suricates the cost seems to be borne by the pup guard only, this
cost has been shown to increase as group size decreases. Because the
probability of leaving a pup guard does not increase with group size in
suricates, each individual will perform this costly task more often in small
groups (Clutton-Brock et al.,
1998).
For all the above reasons, it appears sensible to predict that in Lycaon the cost of leaving a pup guard will be higher for small packs, and that the smallest packs may not be able to afford such cost. As a consequence, smaller packs may be confronted with a trade-off of allocation: either leave a pup guard and suffer reduced provisioning efficiency, or do not and suffer increased pup mortality through predation, loss or drowning. Alternatively, adults might compensate for the lesser amount of food obtained from a hunt by increasing the number of daily hunts, but this then increases costs and risks associated with the hunt. The aim of this article is to explore this trade-off. It may be worth emphasizing at this point that we entirely agree that small packs may sometimes do fine, especially when they involve experienced individuals. There are some good anecdotes of small packs breeding and even pairs or single dogs surviving for some time. Our point is a different one—namely that statistically the break point between success and failure hovers around a pack size threshold, in this case around five adults: the breeders and around three helpers.
Because pup-guarding is well suited to illustrate the probable Allee effect
in Lycaon, it provides an interesting example of the importance of
pack size for the survival of this species. In a previous work, we provided
evidence from the literature of the likelihood of a minimum pack size in
Lycaon (Courchamp and Macdonald,
2001). In addition, we provided a mathematical model of the
dynamical consequences such an effect would have, and showed that the
existence of this threshold increased the probability of extinction at both
the pack and population levels (Courchamp
et al., 2001). These two previous papers highlighted the
importance of this threshold for the conservation of this species, but the
illustration of the mechanism through which the behavior could act on
population dynamics remained to be presented. Here, we do so by presenting a
simple model that describes how the presence of a pup guard imposes an
energetic constraint at pack level and how this cost is related to pack size.
We first test the results of this model by analyzing published data on
pup-guarding. Finally, we present new empirical data from the Hwange
population of Lycaon in Zimbabwe, which confirm the importance of
pack size for pup-guarding, and which support the proposition that there is a
threshold pack size beneath which pup-guarding may become unsustainable.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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Model
We construct a simplistic model, which features the main processes contributing to the energetic costs to Lycaon of pup feeding: amount of food needed for each individuals and amount of food obtained from a hunt by each hunter. For the sake of simplicity, we will assume that yearlings are equivalent to adults in the model. We will therefore only distinguish between adults and pups. That yearlings are less efficient at hunting and maybe less generous in terms of regurgitation will only underestimate the importance of pack size in our model, thereby strengthening our conclusions (but see discussion). For the model, as well as the empirical data below, we define a hunt as the period during which the dogs are away from the den and involved in any phase of hunting activity. A hunt can thus include multiple kills (two hunts are counted if the hunters come back to the den in between); it corresponds to a foraging period of about 3.5 h (sensu Gorman et al., 1998
). Calling
r the gut content of each adult, we consider that a pack of A adults will
provide regurgitated food from a hunt in sufficient amount for P pups and
themselves if and only if rA 
Pep + Aea where
ep and ea are the food requirements of pups and adults,
respectively. Then, if one of the adults acts as a pup guard, A-1 adults bring
back food to the den, and they have to share r(A-1) between the same number of
individuals. We also assume that an adult which guards the pups has a lower
energy requirement than the hunting adults. If we call eg the food
requirement of the pup guard, leaving a pup guard at the den while hunting is
energetically profitable only if the amount brought back by A-1 hunters [thus
r(A-1)] is at least equal to the needs of P pups (thus Pep), plus
the needs of these A-1 hunters [thus (A-1)ea] and those of the pup
guard (eg). We can deduce the number of adults A needed for the
energetic balance to be positive:
 | (1) |
; also used in Carbone et
al., 1997). The amount needed for an adult is considered to be
between 2.5 and 3.5 kg (Gorman et al.,
1998) or between 2 and 2.5 kg
(Creel and Creel, 1995). We
consider in our numerical illustration of Equation 1 that for each of these
two ranges, the lower value corresponds to the metabolic need of a dog with
low energy requirement (pup guard, if it is not at the same time suckling the
pups), while the upper value is needed to achieve energy balance for the
individuals participating in hunts, which involves a higher daily energy
expenditure. One can alternatively consider that this lower value corresponds
to the lesser amount of food provided by regurgitation to the pup guard,
regardless of its energy requirement
(Malcolm and Marten, 1982
showed that pup guards often get a lesser amount of regurgitate). It has been
estimated that, on average, each adult regurgitates about 1 kg of meat after a
full meal (Malcolm, 1979, in
Fuller and Kat, 1990). This
coincides with the values of 4.4 kg for gut content and 3.5 kg eaten per adult
per day. Since it is not specified whether the 1 kg of meat regurgitated is
for one or several pups, we will assume here that it is for one pup only
(taking half this value provides essentially the same results). As a first
step, we consider that dogs always obtain the maximum amount of meat from the
hunt (in terms of prey availability and hunting success), since they are
considered excellent hunters (Creel and
Creel, 1998; Fanshawe and
Fitzgibbon, 1993; Fuller and
Kat, 1993). We use the conversion factor of 6862 kJ/kg of meat
obtained by Creel (1997), to
express our results in energy units.
The previous relationship (Equation 1) provides the minimum number of
adults necessary in a pack for the use of a guard during a hunt not to be
energetically detrimental. However, smaller packs might compensate for this
disadvantage in numbers by hunting more often. We thus modify Equation 1 in
order to account for the potential to increase the amount of food brought to
the den by hunting several times a day: H is the number of hunts performed by
a pack per day. By one hunt we actually mean here one foraging period: one
hunt can involve multiple kills, as is often observed for large packs
(Creel and Creel, 1995). In
addition, the amount of food obtained by each dog should be modified to
account for the differential foraging success (including efficiency of
capture, kill and evisceration of prey and defense of carcass) of
Lycaon in small and in large packs (Creel and Creel,
1995,
1996). For this, we consider
that this amount is a function of the number of adults A and we use the data
of Creel (1997) linking
foraging success (in kJ/dog/day) to the number of adults in the pack. Equation
1 becomes:
 | (2) |
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) to a model of the form:
 | (3) |
level of 0.001 for 
= 12826; ß = 1.24 and µ = 3.58
(Figure 1).
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Field data
The empirical study was conducted by one of us (GR) between April 1994 and
October 1999 in Hwange and adjacent areas totaling 5500 km2. Focal
packs were those that either resided entirely in areas contiguous with the
park or had their home range within a 60 km zone on the park border. Lions and
hyaenas were present throughout the study area. Data came from 13 denning
period events from eight packs, a pack being defined as a potential breeding
unit containing at least one adult of each sex
(Malcolm, 1979;
Reich, 1981). We avoided
pseudoreplication by comparing results among packs (observations averaged
within packs). Denning period is when the pups are too young to follow the
adults during long trips, and the pack exhibits refuging rather than nomadic
behavior. This period is of about 12 weeks. Pup caching occurs when pups are
12 weeks old at least and the pack is mobile. Since the pups are too young to
follow the pack all day long, they are hidden during some foraging periods.
Our data set includes this event as pup-guarding occurs when pups are cached
as well. In all instances of pup caching the data were obtained by remaining
with the pups.
Dogs were categorized into age classes as follows: pups (<1 year old),
yearlings (1-<2 y.o.) and adults (2 y.o.). Pups were identified at
emergence providing a record of the number of dogs in each class category at
all times. In six packs, data were obtained through radio-collared
individuals, either by following packs on hunts to see which individuals were
hunting, or by den watching. The latter was used only on packs that had been
followed for more than 9 months and were deemed habituated to observer
presence at this critical time. Individuals were radio-collared when
conditions were favorable in terms of habitat density and time of day. In
thicker bush the anaesthetic doses were kept at the higher end of the range
specified to reduce knockdown time and thus the likelihood of an individual
being darted and subsequently lost. Capture was not undertaken if the risk of
the animal being lost was too important (thick bush). Immobilization was only
undertaken in the mornings in order to reduce predation risk (dogs are more
vulnerable at night, and by that time they should have completely recovered
from anesthesia). Only adults over the age of 14 months were collared, with
the first individual to be collared being selected at random. When a second
radio collar was put on a pack, an adult of the opposite sex was usually
selected. Retroreflective protective collars, which often had no radio unit
were fitted to any individual that could be immobilized providing they were
old enough. These collars, though fitted in an attempt to reduce road
mortality, helped to reveal which individuals were hunting/pupguarding at
night. Proven breeding alpha females were never collared because Ketamine is
known to cross the placental barrier, though one female subordinate at the
time of collaring, subsequently acquired alpha status. No pup-guarding data
are presented within 5 days after collaring.
All dogs were chemically immobilized using a 5.5:1 Ketamine HCl (Fort Dodge): Xylazine (Bayer). Administration of the drug was intramuscular in the rear quarter by dart (n = 9). Darting was achieved using 1.8 mm Daninject darts and a 1M rifle with doses ranging from 180 mg:33 mg to 220 mg:40 mg depending on age, condition, and size. All procedures on anaesthetized animals were carried out in situ with the dogs being laid onto a canvas reserved solely for this purpose. As the depth of anesthesia could not be measured, precautions were taken to reduce possible stress from awareness of close proximity with humans. These measures involved the dogs being blindfolded and fitted with earmuffs specially designed to allow easy removal by the study animal in case of a bolt recovery. Also communications were kept silent and carried out by predetermined hand signals. As frequently other members of the pack were waiting close by, personnel assisting adopted no erect postures. When vital reflex signs indicated that the Ketamine (the half-life of which is considerably shorter than Xylazine) was nearly metabolized, immobilization was reversed, using 4-6 mg of Antipamezole (Pfizer) administered intramuscularly.
All immobilized dogs were monitored for 24 h post anesthesia to ensure their safe return and integration into their pack. The knockdown time ranged from 45-95 min (mean 65 min). Recovery was seemingly full by the late afternoon prior to the evening hunt. Response to the collar by the wearer was indifference. Any pups in the pack would show interest in the collar, however this interest would wane to none after 7-10 days. There was no other observable effect of the collars. Protective collars remained on individuals, with MOD 400 collars being replaced with Sirtrack collars where possible. No hair slip was noted with protective collars and minimal slip was noted in MOD 400 collars.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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Model
Figure 2 shows the predicted minimum number of adults needed to both feed the pups from the product of one hunt and guard them during this hunt. This shows that, in theory, packs of five adults cannot feed pups sufficiently if they are to use one hunter as a pup guard. This however does not account for the higher foraging success of large hunting parties, which could increase the difficulty of leaving a guard in small packs. We take this into account by replacing the constant amount of food obtained for a hunt, by a function of the hunting party size (Equation 3 and Figure 1). We use the model of Equation 3 in Equation 2 to express the number of hunts H that must be completed to feed a pack with P pups, A-1 hunters and one pup guard. We first show the number of hunts that must be achieved in theory for a pack of a given size to be able to feed a litter of a given size (Figure 3a). This figure also shows how, regardless of the use of a pup guard, smaller packs will have to increase the number of hunts (and the associated costs and risks) to raise the same number of pups as do larger packs.
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It is then possible to calculate the number of additional hunts that must
be performed to compensate for the absence of one hunter which stays to
protect the pups at the den:
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Although we do not aim to provide an accurate estimate of the number of
hunts needed to compensate for pup-guarding, it would be interesting at this
point to estimate how many times a day a Lycaon is able to hunt. In a
previous study, the maximum number of hunts per day was eight
(Creel and Creel, 1995).
Although this may only reflect the number of hunts that dogs need to satisfy
their requirements, eight hunts per day might be close to a maximum a dog can
sustain. This number is however less than our prediction of the number
required by the smallest packs to compensate for the use of a pup guard
(Figure 3). A recent analysis
of the energetic constraints of hunting showed that hunting for an average of
3.5 h daily, Lycaon is already close to its physiological limits
(Gorman et al., 1998). It may
be difficult to equate time spent hunting and number of hunts in those two
studies, but, clearly, small groups may be unable to cope with the number of
additional hunts required daily to compensate for the loss of a hunter, and
may instead forgo pup-guarding.
Literature data
We re-analyzed some of the results of a published study of a Tanzanian
population of Lycaon (Malcolm and
Marten, 1982). This study presented the distribution of
pup-guarding occurrences for the different members of five studied packs.
Since the numbers of adults was similar for each pack (there were no yearlings
these years), we plotted the number of pup-guarding occurrences against the
ratio of adults over pups (Figure
4). This figure shows a nonlinear relationship, significant at the
level of 0.001, between ratio of adults over pups in the pack and
occurrence of pup-guarding. It is interesting in this regard to observe that
there seems to be a threshold set slightly under two pups per adult, below
which pup-guarding becomes much less likely. If one takes 10.31 as the average
litter size (calculated over 165 litters from published data:
Burrows et al., 1994;
Fuller et al., 1992;
Maddock and Mills, 1994), then
this threshold is under 5.16 adults. This is suggestive of a cost of
pup-guarding when fewer adults are in charge of more pups. This analysis
supports the prediction of our model. In a given ecosystem and for the same
years, packs where adults had to feed fewer pups more often used a pup guard
than did other packs. Note however that few packs were available for this
analysis, and all were of a rather small size (four or five adults).
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Field data
For this analysis we used results from a different population, in Zimbabwe.
Pack size and pup-guarding status was known for 246 hunts out of a potential
of 314 hunts for the 13 denning periods. Of these, 33% were undertaken by the
whole pack, the remaining 167 hunts involving one pack member as a pup guard.
Hunts that took place during the night (22 hunts), that is when the risk of
pup predation is high, invariably involved a guard remaining with the pups,
whereas pups were left alone during 39% of diurnal hunts
(
12 = 11.709; p =.0006). Furthermore,
pup-guarding was significantly more likely in larger packs: the eight packs of
less than five individuals left a guard with the pups in 34.7 ± 0.1% of
their hunts, while the five packs of more than five individuals left a guard
in 88.5 ± 0.1% of their hunts (Mann-Whitney Z = -2.635;
p =.0084).
We tested the effect of both time of hunt (day or night) and pack size on
the probability of pup-guarding through a logistic regression (binomial
error), creating ad hoc groups for each size-pack (18 groups).
Probability of pup-guarding strongly differed between groups
(172 = 17.90; p < 10-4).
This difference between packs is explained by their size (size nested within
group, F161 = 9.25; p =.008). In
addition, probability of pup-guarding differed between hunting periods (a.m.,
p.m., and night, 22 = 11.67; p =.003). The
effect of hunting period on probability of pup-guarding was the same between
group (interaction group—hunting period, 112
= 17.90; p =.08). The distribution of the pup-guarding occurrences
for packs of different sizes is shown in
Figure 5. The largest
difference in the number of hunts with or without pup-guarding was between
packs of five or less and packs of more than five dogs
(12 = 89.345; p < 10-4),
suggesting once more a threshold of five individuals for pup-guarding in
Lycaon. When a distinction was made between yearlings and adults, the
significant effect of pack size on the probability of pup-guarding was lost if
yearlings were not taken into account, probably because too few packs were
available. The presence of yearlings in the pack was however a significant
predictor of the probability of pup-guarding (Mann-Whitney Z =
-2.143; p =.0321). To facilitate comparison between our data and that
published by Malcolm and Marten
(1982), we explored the effect
of the ratio of pack size (adults plus yearlings, when present) to number of
pups. We found that there was a highly significant difference between packs
with a ratio below 0.5 (29.8% of pup-guarding) and packs with a ratio above
0.5 (75.5% of pup-guarding; 12 = 35.664; p
< 10-4). Pup-guarding occurrences were too few for small pack
sizes to test whether small packs undertook more daily hunts if they used a
pup guard than if they did not use one. Packs of three never left a pup guard,
which supports the prediction of our model, although the lack of observation
of the pups of one of the packs of three during their first weeks may account
in part for this result. Results for packs of four and five were not
significant. However, packs of two performed 11 times an additional hunt over
the 18 days when they left a pup guard, compared with no additional hunt for
the 12 days when they did not leave a guard, which makes a significant
difference (12 = 11.579; p =.0007). This
result confirms our prediction of a high cost of pup-guarding for small
packs.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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Combining theoretical and empirical approaches, we showed that in Lycaon, leaving or not leaving a pup guard amounts to choosing between two costs. The absence of a pup guard may risk high pup mortality, whereas presence of a pup guard may lead to higher mortality through lost hunting efficiency. In small packs, employing a pup guard during the hunt may result in crucially diminished amounts of food brought back to the den by the remaining adults. Consequently, adults in small packs may have to complete additional costly and risky hunts each day to compensate for the loss of a hunter to pup-guarding. Yet, dispensing with a pup guard may be hazardous as it is generally agreed that pup guards have the potential to prevent loss of pups and pup predation. High mortality of pups (around 40%) by predation from intraguild competitors has been reported in several studies (van Heerden et al., 1995
;
Ginsberg et al., 1995;
Mills and Gorman, 1997).
Although logistically difficult, it would be interesting to collect enough
observational data to be able to test the extent to which pup mortality
changes with the presence or absence of a guard, controlling for pack size.
Here we show that a pup guard was systematically used during hunts at night,
when lions and hyaenas are active and a threat to unattended pups. We
demonstrate theoretically that using a pup guard is costly in terms of energy
for the whole pack, and that only large packs, or packs with few pups, can
afford it. We also show that smaller packs need to hunt more often to feed
their pups, especially when using a pup guard.
The simplistic mathematical model we used here indicated a relationship
between pack size and energetic cost involved with pup-guarding. Yet, in this
model, many points could be improved. For example, we focused on pack size
only, but individuals that have different social status will have different
individual costs and benefits at guarding the pups of the pack breeders.
Similarly, we did not focus on the precise value that should be taken by the
amount eaten by the guard. As shown by Malcolm and Martens (1982), the guard
often eats less that the other adults, or even not at all in some cases. In
that case, the lower value used for the amount eaten by the guard does not
reflect its energy requirement (especially if it is the lactating mother). As,
in this case, the cost of pup-guarding is also borne by the guard itself, a
need for more food that may prevent individuals from pup-guarding as much as
they would in absence of this food stress. To be more realistic, our model
should have used a larger value for eb. However, doing so would
lead to an exacerbation of the effect we predict in this paper, which only
strengthens our point. It also is noteworthy that we hypothesized that only
one guard was left at a time, regardless of the number of pups. A more
realistic alternative might be to consider that very large litters would
require two or more simultaneous guards, and that this could be afforded only
when the pack size is sufficiently high. This possibility, which has been
observed in the wild (Malcolm and Marten,
1982), would also increase the trade-off between pup-guarding and
hunting. Note that if a linear relationship was used instead of the model used
in Equation 3 for the foraging success of A hunters, the results would be
qualitatively unchanged and would quantitatively more strongly emphasize the
importance of pack size.
Re-analysis of published data showed a positive relationship between the
occurrence of pup-guarding and the ratio of adults to pups, partially
confirming the prediction of our mathematical model. An analysis of new
empirical data completes this, by confirming the relationship between pack
size and the probability of pup-guarding. These analyses also show that
yearlings play an important role in this regard, which supports our pooling of
adults and yearlings in the model. It is interesting to note that Burrows
(1995) also found an effect of
pack size on pup survival, which was significant only if yearlings were taken
into account. Although yearlings are not yet experienced hunters, their
presence contributes to foraging efficiency. It is generally the alpha male or
the alpha female which leads the hunt, but yearlings nonetheless contribute to
several aspects of cooperative hunting, including the diminution of
kleptoparasitism, by decreasing the carcass access time (increased cleaning
efficiency) and increasing the ratio of dogs/hyaenas (see
Carbone et al., 1997;
Fanshawe and Fitzgibbon,
1993). In addition, by regurgitating meat to the begging pups back
at the den, (Estes and Goddard,
1967; Malcolm and Marten,
1982), yearlings' stomachs can act as "the storage and
preparation containers for the pups' food"
(Kühme,
1965). This also allows a rapid "transport of the hastily
dismembered prey into safe cover"
(Kühme,
1965). For these reasons, the pack may chose to use a pup guard
when the cost of doing so is offset to the presence of yearlings to increase
the hunting party.
Another solution enabling the adults to lower the costs of this trade-off might be to alternate strategies. If pup-guarding is used only occasionally (e.g., only if a predator is around or in case of heavy rains, when the pups risk drowning in the den), this may lower the risk of pup mortality, while avoiding under-nourishment (or hunting injuries). By constantly adjusting their strategy, adults may be able to feed sufficiently all pack members as often as possible, thereby maintaining all dogs in good condition, so that when a pup guard must be used, the associated loss of energy (less food or more hunts) is not too costly. Therefore, we predict that pup guards should be used for only a proportion of the hunts, and this proportion should increase with pack size. Both the published literature and our data suggest that this is indeed the case.
We approached this problem through four independent analyses, and each led
to the same estimate of a critical threshold around five adults (see Figures
2,
3b,
4, and
5). Of course, the
simplifications involved mean that we do not expect our estimates to be
precise values of the number of adults needed for a pup guard to be
affordable. Similarly, the number of additional hunts is given as only an
indication of a likely process. Individual differences, such as the experience
of hunters (the pup guard is often the mother and it is also often one of the
most experienced hunters), and the environment (prey availability and
characteristics of the habitat) are major factors that will change these
values. Our main aim has been to demonstrate that a threshold pack size
exists, rather than to be precise about its value. Yet it is striking that, as
was the case with four approaches used independently in this article, other
authors have reported that packs of more than four to six Lycaon have
advantages over smaller packs (Carbone et
al., 1997; Creel et al.,
1998; Estes and Goddard,
1967; McNutt,
1996).
As Lycaon is among the most endangered canid species
(Woodroffe and Ginsberg,
1997), our findings have noteworthy implications for their
conservation biology. This is particularly pertinent as this species is a
victim of negative attitudes (Rasmussen,
1999) and anthropogenic mortality, the impact of which has the
capacity to reduce numbers to below a sustainable threshold and where the loss
of one or two individuals can impact on pack integrity and ability to survive
(Rasmussen, 1996,
1997). The relationship
between survival and group size, upon which this work is focused, is not
specific to Lycaon, nor is pup-guarding the sole aspect to which such
a trade off may apply: this concept could also be applied to other cooperative
breeders, many of which are also vulnerable to extinction and currently
endangered.
|
ACKNOWLEDGEMENTS |
|---|
This work was supported by a TMR 30 Marie Curie Fellowship from the European Community (FC). The authors wish to thank the Director of the Department of National Parks and Wildlife Management of Zimbabwe and staff for permission to conduct research on this endangered species and assistance given during the field study, as well as Tim Clutton-Brock for inspiring discussions about the likelihood Allee effect in obligate cooperative breeders. We are also grateful to him and to Andrew Balmford, Scott Creel, Andy Russell, and an anonymous referee for critical reading of the manuscript.
|
REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Burrows R, 1995. Demographic changes and social consequences in wild dogs, 1964-1992. In: Serengeti II. Dynamics, management and conservation of an ecosystem (Sinclair ARE, Arcese P, eds). Chicago: University of Chicago Press; 385-400.
Burrows R, Hofer H, East ML, 1994. Demography, extinction and intervention in a small population—the case of the serengeti wild dogs. Proc Roy Soc Lond B 256: 281-292.[Medline]
Carbone C, DuToit JT, Gordon IJ, 1997. Feeding success in African wild dogs: Does kleptoparasitism by spotted hyenas influence hunting group size? J Anim Ecol 66: 318-326.
Childes SL, 1988. The past history, present status and distribution of the hunting dog Lycaon pictus in zimbabwe. Biol Cons 44: 301-316.
Clutton-Brock TH, 1991. The evolution of parental care. Princeton, New Jersey: Princeton University Press.
Clutton-Brock TH, Brotherton P, Smith R, McIlrath GM, Kansky R, Gaynor D, O'Riain J, Skinner JD, 1998. Infanticide and expulsion of females in a cooperative mammal. Proc Roy Soc Lond B 265: 2291-2295.[Medline]
Clutton-Brock TH, Gaynor D, McIlrath GM, MacColl A, Kansky R, Chadwick P, Manser M, Skinner JD, Brotherton PNM, 1999. Predation, group size and mortality in a cooperative mongoose, Suricata suricatta. J Anim Ecol 68: 672-683.
Courchamp F, Clutton-Brock TH, Grenfell BT, 1999. Inverse density dependence and the Allee effect. Trends Ecol Evol 14: 405-410.[Medline]
Courchamp F, Clutton-Brock TH, Grenfell BT, 2000. Multi-group dynamics and Allee effects in the African wild dog Lycaon pictus. Anim Cons 3: 277-285.
Courchamp F, Macdonald DW, 2001. Crucial importance of pack size in the African wild dog Lycaon pictus. Anim Cons 4: 169-174.
Creel S, 1997. Cooperative hunting and group size: assumptions and currencies. Anim Behav 54: 1319-1324.[Web of Science][Medline]
Creel S, Creel NM, 1995. Communal hunting and pack size in african wild dogs, Lycaon pictus. Anim Behav 50: 1325-1339.
Creel S, Creel NM, 1996. Limitation of African wild dogs by competition with larger carnivores. Cons Biol 10: 526-538.
Creel S, Creel NM, 1998. Six ecological factors that may limit African wild dogs, Lycaon pictus. Anim Cons 1: 1-9.
Creel S, Creel NM, Monfort SL, 1998. Birth order, estrogens and sexratio adaptation in African wild dogs (Lycaon pictus). Anim Reprod Sci 53: 315-320.[Medline]
Doolan SP, Macdonald DW, 1999. Co-operative rearing by slendertailed meerkats (Suricata suricatta) in the Southern Kalahari. Ethology 105: 851-866.
Estes RD, Goddard J, 1967. Prey selection and hunting behavior of the African wild dog. J Wildl Manage 31: 52-70.
Fanshawe JH, FitzGibbon CD, 1993. Factors influencing the success of an African wild dog pack. Anim Behav 45: 479-490.
Fanshawe JH, Frame LH, Ginsberg JR, 1991. The wild dog: Africa's vanishing carnivore. Oryx 25: 137-146.
Fuller TK, Kat PW, 1990. Movements, activity, and prey relationships of African wild dogs (Lycaon pictus) near aitong, southwestern Kenya. Afr J Ecol 28: 330-350.
Fuller TK, Kat PW, 1993. Hunting success of African wild dogs in southwestern Kenya. J Mammal 74: 464-467.
Fuller TK, Kat PW, Bulger JB, Maddock AH, Ginsberg JR, Burrows R, McNutt JW, Mills MGL, 1992. Population dynamics of African wild dogs. In: Wildlife 2001: populations (McCullough DR, Barrett RH, eds). London: Elsevier Applied Science; 1125-1139.
Ginsberg JR, Alexander KA, Creel S, Kat PW, McNutt JW, Mills MGL, 1995. Handling and survivorship of African wild dog (Lycaon pictus) in five ecosystems. Cons Biol 9: 665-674.
Ginsberg JR, Macdonald DW, 1990. Foxes, wolves, jackals and dogs: an action plan for the conservation of canids. Gland, Switzerland: International Union for the Conservation of Nature and Natural Resources.
Gorman ML, Mills MG, Raath JP, Speakman JR, 1998. High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391: 479-481.
Jennions MD, Macdonald DW, 1994. Cooperative breeding mammals. Trends Ecol Evol 9: 89-93.
Kühme W, 1965. Communal food distribution and division of labour in African hunting dogs. Nature 205: 443-444.[Medline]
Maddock AH, Mills MGL, 1994. Population characteristics of African wild dogs Lycaon pictus in the eastern transvaal lowveld, South-Africa, as revealed through photographic records. Biol Cons 67: 57-62.
Malcolm JR, 1979. Social organisation and the communal rearing of pups in African wild dogs (Lycaon pictus) (PhD Dissertation). Cambridge: Harvard University.
Malcolm JR, Marten K, 1982. Natural-selection and the communal rearing of pups in African wild dogs (Lycaon pictus). Behav Ecol Sociobiol 10: 1-13.
McNutt JW, 1996. Adoption in African wild dogs, Lycaon pictus. J Zool 240: 163-173.
Mills MGL, Gorman ML, 1997. Factors affecting the density and distribution of wild dogs in the Kruger National Park. Cons Biol 11: 1397-1406.
Rasmussen GSA, 1996. Predation on bat eared foxes Otocyon megalotis by Cape hunting dogs Lycaon pictus. Koedoe 39: 127-129
Rasmussen GSA, 1997. Conservation status of the painted hunting dog Lycaon pictus in Zimbabwe. Ministry of Environment and Tourism, Department of National Parks and Wildlife Management, Zimbabwe.
Rasmussen GSA, 1999. Livestock predation by the painted hunting dog Lycaon pictus in a cattle ranching region of Zimbabwe: a case study. Biol Cons 88: 133-139.
Reich A, 1981. The behavior and ecology of the African wild dog (Lycaon pictus) in the Kruger National Park (PhD Dissertation). New Haven, CT: Yale University.
Solomon NG, French JA, 1996. Cooperative breeding in mammals. Cambridge: Cambridge University Press.
Stephens PA, Sutherland WJ, 1999. The Allee effect and its consequences for ecology and conservation. Trends Ecol Evol 14: 401-405.[Medline]
van Heerden J, Mills MGL, van Vuuren MJ, Kelly PJ, Dreyer MJ, 1995. An investigation into the health status and diseases of wild dogs (Lycaon pictus) in the Kruger National Park. J S Afr Vet Med Assoc 66: 18-27.
Woodroffe R, Ginsberg JR, 1997. Past and future causes of wild dogs' population decline. In: The African Wild Dog. Status Survey and Conservation Action Plan (Woodroffe R, Ginsberg JR, Macdonald DW, and the IUCN/SSC Canid Specialist Group, eds). Gland, Switzerland: IUCN; 58-74.
Woodroffe R, Ginsberg JR, 1999. Conserving the African wild dog Lycaon pictus. I Diagnosing and treating causes of decline. Oryx 33: 132-142.
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