Biological Conservation 115 (2003) 319–327

www.elsevier.com/locate/biocon

Can small, isolated primate populations be effectively reinforced

through the release of individuals from a captive population?
Adam Britta,*, Charles Welchb, Andrea Katzb,c
a
Madagascar Fauna Group, 1 Zoo Road, San Francisco, CA 94132, USA
b
Madagascar Fauna Group, BP 442, Toamasina 501, Madagascar
c
Duke University Primate Center, 3705 N. Erwin Road, Durham, NC 27705, USA

Received 4 October 2002; received in revised form 4 March 2003; accepted 18 March 2003

Abstract
Since November 1997 the Madagascar Fauna Group (MFG) has released 13 captive-bred black and white ruffed lemurs (Varecia
variegata variegata) into the Betampona reserve in eastern Madagascar. Five of the thirteen are currently surviving, including one
male who has integrated into a wild group. Five of the released lemurs fell victim to predation by fossa (Cryptoprocta ferox), one
died of malnutrition, one disappeared from the reserve and one was withdrawn from the release programme. Ten of the released
lemurs survived for more than one year post release, although all required varying levels of supplementary feeding. One pair bred
twice—the first time the infants did not survive, but on the second occasion triplets were successfully raised beyond weaning. One of
the triplets (male) is still surviving. One male has integrated into a wild group and sired a single infant in 2002 and a female released
in 2001 gave birth to twins sired by a wild male also in 2002. The release programme has thus achieved a major objective of rein-
forcing the existing wild population. To date there is no significant difference in survival rates between animals born and raised in
free-ranging environments and those raised in cages, between animals greater than or less than 5 years old at time of release, or
between males and females.
# 2003 Elsevier Ltd. All rights reserved.
Keywords: Re-introduction; restocking; Varecia; Conservation; Cryptoprocta; Captive-breeding

1. Introduction case in Brazil’s Atlantic coastal forest in the late 1970s

The idea of breeding animals in captivity for eventual
release into the wild is a major aim of modern zoologi-
cal collections (Durrell and Mallinson, 1987). The basic
philosophy of captive breeding for conservation is that
the captive population forms part of a metapopulation,
i.e. the total population in captivity and in the wild, and
both are managed interactively to increase the persis-
tence time of the species (Seal et al., 1994).
With the human population ever increasing, more and
more of the natural environment is being destroyed,
especially in the tropics. At best only small, isolated
fragments of more or less intact habitat remain: islands
amongst an ocean of human devastation. Such was the
* Corresponding author. Present address: Herbarium, Royal Bota-
nic Gardens, Kew, Richmond, Surrey TW9 3AB, UK. Tel.: +44-20
8332-5265; fax: +44-20-8332-5278.
E-mail address: a.britt@rbgkew.org.uk (A. Britt).
0006-3207/03/$ - see front matter # 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0006-3207(03)00150-2
(Coimbra-Filho and Mittermeier, 1977). However, one
small primate species was to become a symbol of hope
for the conservation of this habitat, and for the role of
captive-breeding in conservation. The golden lion
tamarin (Leontopithecus rosalia) became the first example
of a ‘flagship species’, a species that promoted conserva-
tion of the Atlantic coastal forest ecosystem as a whole
(Mittermeier, 1986, 1988). In the late 1970s the total wild
population of golden lion tamarins was estimated at
100–200 individuals (Coimbra-Filho and Mittermeier,
1977). The first re-introductions of captive-bred animals
took place in the mid-80s (Kleiman et al., 1986). By
1989, 71 animals had been released, 27 survived (38%)
and 26 more were born to the released animals (Beck et
al., 1991). By 1994 it was estimated that a wild popula-
tion of 450 existed with an additional 550 in captivity
(Dietz et al., 1994).
Just as the golden lion tamarin served as a flagship
species for the conservation of an entire ecosystem in
320 A. Britt et al. / Biological Conservation 115 (2003) 319–327
Brazil, it was hoped that the black and white ruffed
lemur (Varecia variegata) could serve the same role for
the eastern rain forest of Madagascar. A large captive
population of Varecia, from 21 founders, had been well
managed since the 1960s (Porton, 1992). Thus in the
early 1990s the Madagascar Fauna Group (MFG),
began to concentrate their efforts towards an experi-
mental re-stocking of Varecia into the Betampona
Reserve. Betampona is one of the few fragments of the
once extensive eastern lowland rain forest. It provides
refuge for 11 lemur species, including the indri (Indri
indri), simpona (Propithecus diadema diadema) and
aye-aye (Daubentonia madagascariensis). Surveys in
1990 and 1991 estimated the wild Varecia population
at 35 individuals (Welch and Katz, 1992), too small to
be viable in the long-term (Franklin, 1980). The
results of population simulation modelling exercies
indicated that the long-term viability of the Betam-
pona Varecia sub-population would be significantly
enhanced by the release of a relatively few individuals
from the captive sub-population (Seal, 1997). How-
ever, the question remained as to whether such ani-
mals could adapt to life in the wild, integrate and
ultimately reproduce with the existing Varecia sub-
population.
There is evidence to suggest that animals bred in cap-
tivity may lose the skills and abilities necessary for sur-
vival in the wild (Frankham et al., 1986). In fish, for
example, there is strong evidence of genetic adaptation
to the captive environment (e.g. Johnsson and Abra-
hams, 1991), presumably effected by relaxation in selec-
tive pressures. Evidence for mammalian species is
mainly anecdotal (Price, 1984; Frankham et al., 1986),
but if physical and social environments differ con-
siderably from those in nature it can be predicted that a
similar phenomenon may occur.
Problems associated with the release of captive-bred
mammals were experienced in the golden lion tamarin
re-introduction programme (Kleiman et al., 1986).
Many of the animals that were released were unable to
perform key natural activities adequately. Conversely
captive-bred brush-tailed phascogales (Phascogale
tapoatafa) re-introduced to the wild encountered no
such problems (Soderquist and Serena, 1994). In general
very low survival rates are reported for untrained cap-
tive-reared animals released in nature (e.g. Wood-Gush
and Duncan, 1976).
Research into animal domestication exposes a num-
ber of potential problems facing captive-breeding and
subsequent re-introduction of endangered species.
Compared with the wild, captive animals experience
different resources, limitations to physical and psycho-
logical space, the inability to express behaviours fully
and the proximity of objects formerly associated with
fear (Kohane and Parsons, 1988). The first indication of
evolutionary change under domestication is likely to be
behavioural (Mayr, 1963). This is as a consequence of
relaxed selection for some traits as certain behaviours
important for survival in the wild tend to lose their sig-
nificance in the artificial, captive environment. Captive-
breeding for conservation is comparable to the early
stages of domestication. Thus, behavioural change
should be expected, and behaviour may depart further
from that in natural conditions as the number of cap-
tive-born generations increases. Kummer and Kurt
(1965) found that wild hamadryas baboons (Papio
hamadryas) exhibit behaviours not observed in captiv-
ity, and vice versa (see also Klein and Klein, 1971 for
the spider monkey, Ateles geoffroyi). However, there is
little or no evidence that domestication has caused
behaviours to be eliminated or that the basic structure
of motor patterns for behaviour has been altered
(Miller, 1977). Encouragingly for captive-breeding pro-
grammes, the characteristic perceptual capabilities of
most species seem to remain highly stable under
domestication (Kretchmer and Fox, 1975; Heaton,
1976). Behavioural differences between wild and
domestic stocks are quantitative in character and best
explained by shifting thresholds based on genotypic
changes, the effects of the captive environment on
behavioural development, or both (Price, 1984). Early
experience appears to be more important than the
effects of domestication in the development of beha-
viours, for example, antipredator behaviours (Spiegel et
al., 1974).
The evidence above suggests that special efforts will
be required to maintain the behavioural skills necessary
for survival in the wild within a captive sub-population.
Originally a welfare issue, environmental enrichment
has, with the realisation of the potential role of zoos in
conservation, become vital for the maintenance of nat-
ural behaviour in captive populations (Shepherdson,
1994). Increasingly, the importance of providing
endangered species in captivity with naturalistic envir-
onments, allowing the expression of a full range of nat-
ural behaviours, has been realised.
This paper will examine if captive-bred Varecia retain
the skills to survive in the wild, and compare the effects
of differing captive conditions on the ability to adapt to
their natural habitat. The implications of the findings
from this study for the future of captive-breeding for
conservation will be discussed.
2. Methods
2.1. Study site
The Betampona Reserve is situated between 17
150 –
17
550 S and 49
120 –49
150 E about 40 km north-west of
the major port of Toamasina on the east coast of
Madagascar. Betampona covers an area of 2228 ha with
 A. Britt et al. / Biological Conservation 115 (2003) 319–327
altitude ranging from 275 to 650 m above sea level
(Razokiny, 1985). The climate is humid tropical with a
mean annual rainfall of 2857 mm from 1998 to 2001.
There are no dry months; rainfall peaks from January
to March and June to August, while October and
November are relatively dry. Temperature falls mark-
edly between June and September. The forest at Betam-
pona is dominated by trees of the families Lauraceae,
Moraceae, Euphorbiaceae, Clusiaceae, Sapotaceae, Myr-
taceae, Arecaceae, Liliaceae and Burseraceae; lianas of the
families Dillenidae and Apocyanaceae; and numerous
epiphytes of the families Aspleniaceae and Orchidaceae
(B.R. Iambana, personal communication, Andrianar-
isata, 1995). The canopy height averages 20–25 m and is
very broken, with occasional large emergents of > 30 m.
The terrain is steep with numerous ridges.
2.2. Study animals
Three releases were carried out: November 1997—an
established group from Duke University Primate Center
(three males, two females); November 1998—a male
was released with two females and a third female was
released with a male from 1997; January 2001—a
mother and three offspring (three males, one female)
(Britt et al., 1998, 2000a,b, 2001). The sex ratio of these
groups was force of circumstance, i.e no scientific ration-
ale was involved in the make-up of the three groups.
November was selected as the best time for release being
prior to the cyclone season (January–March) and a time
of good fruit availability. However the third release
took place in January due to a reassessment of release
strategy following significant losses to predation in
2000. A ‘soft’ release strategy was adopted, which
involved the provision of supplementary food in baskets
suspended within the canopy, recapture of individuals if
they strayed from the release area and veterinary assis-
tance if necessary. The cessation of supplementary
feeding for the first release group occurred roughly 2
months post-release as the released lemurs were at the
time completely ignoring the food provided, however it
was reinstated on two later occasions due to concerns
over weight loss. The second release group were provi-
sioned throughout their time in the forest as they were
completely unwilling to range far enough to encounter
sufficient natural food resources. Provisioning for the
third release group was ended 2 months after release–
again they were ignoring the provisioned food provided.
However, it was reinstated during the austral winter
again due to concerns over weight loss. This group has
since survived for over a year without supplementary
food.
The captive-bred Varecia released were considered as
two sets on the basis of experience in free-ranging
environments (Sets 1a and 1b), age (Sets 2a and 2b) and
gender (males and females). (See Tables 1–3)
321
Set 1a: Individuals with considerable experience (at
least 6 months) in a free-range environment during
their early developmental phase.
Set 1b: Individuals with limited experience in a free-
ranging environment. Early development phase spent
in a cage environment.
Set 2a: Individuals less than 5 years old at release.
Set 2b: Individuals more than 5 years old at release.
2.3. Data collection and analysis
Data were collected through long-term monitoring
of the released Varecia by the MFG field team at
Betampona from November 1997 to January 2002.
All the released Varecia were fitted with radio-collars
and comparative detailed behavioural data were col-
lected from both the released and resident wild
Varecia to allow investigation of the adaptation of
the released animals. These data will be presented
elsewhere.
Statistical analyses of the limited data set were
undertaken using SPSS 10.0 for Windows. Mean survi-
val times and standard errors of the mean were calcu-
lated for each group. Survival differences to date
between each pair of groups were investigated for sta-
tistical significance using Mann–Whitney U-tests. Due
to the small sample sizes involved the significance level
was set at P < 0.01 for all tests performed.
3. Results
3.1. Survival
The mean survival time for Set 1a animals was 21.22
months  5.75 versus 20.75 months  1.32 for Set 1b.
The difference in survival time between the two sets was
not significant (U=13.5, z=0.706, exact two-tailed
P=0.503).
The mean survival time for Set 2a animals was 23.60
months  8.33 versus 19.50 months  4.16 for Set 2b.
The difference in survival time between the two sets was
not significant (U=17.5, z=0.372, exact two-tailed
P=0.724).
The mean survival time for males was 25.14
months  5.98 versus 16.00 months  5.71 for females.
The difference in survival time between males and
females was not significant (U=13.5, z=0.657, exact
two-tailed P=0.530).
3.2. Survival without supplementary feeding
The mean survival time without supplementary food
for Set 1a animals was 9.89 months  2.99 versus 4.00
months  2.00 for Set 1b. The difference in survival time
without supplementary feeding between the two sets
322 A. Britt et al. / Biological Conservation 115 (2003) 319–327

Table 1
Details of the nine Set 1a Varecia released at Betampona

Individual Studbook no. Birth date Institution Free-range experience (months) Date of release

Male 1a 536m 24 April 1985 D.U.P.C.b 54 10 November 1997

Male 2 1322m 31 March 1993 D.U.P.C. 43 10 November 1997
Male 3 1745m 14 April 1996 D.U.P.C. 18 10 November 1997
Male 5 1974m 7 May 1999 D.U.P.C. 12 18 January2001
Male 6 2065m 13 May 2000 D.U.P.C. 6 18 January 2001
Male 7 2066m 13 May 2000 D.U.P.C. 6 18 January 2001
Female 1 591f 8 April 1986 D.U.P.C. 138 10 November 1997
Female 2 1120f 3 April 1991 D.U.P.C. 78 10 November 1997
Female 3 1376f 1 May 1993 W.C.S.c St. Catherine’s 15 20 November 1998
a
Born free-range, but removed to cage for 8 years
b
D.U.P.C.=Duke University Primate Center.
c
W.C.S.=Wildlife Conservation Society, St. Catherine’s Island, Georgia.

Table 2
Details of the four Set 1b Varecia released at Betampona

Individual Studbook no. Birth date Institution Free-range experience (months) Date of release

Male 4 1169m 26 April 1991 Los Angeles Zoo 3 25 November 1998

Female 4 1170f 1 May 1991 Hogle Zoo 2 25 November 1998
Female 5 1171f 1 May 1991 Hogle Zoo 2 25 November 1998
Female 6 1382f 2 May 1993 Santa Ana Zoo 24 18 January 2001

Table 3 ferox), accounting for five of the seven losses (Britt et

Individuals in Sets 2a and 2b
Set 2a
Male 2
Male 3
Male 5
Male 6
Male 7
was not significant (U=11.5, z=1.023, exact two-
tailed P=0.330).
The mean survival time without supplementary food
for Set 2a animals was 13.40 months  4.47 versus 4.75
months  1.68 for Set 2b. The difference in survival time
without supplementary feeding between the two sets
approaches significance (U=7.5, z=1.866, exact two-
tailed P=0.065).
The mean survival time without supplementary food
for males was 11.57 months  3.48 versus 2.80
months  1.59 for females. The difference in survival
time without supplementary feeding between males and
females approaches significance (U=3.0, z=2.388,
exact two-tailed P=0.018).
al., 2001) (see Table 4). It is hypothesised that the
Set 2b released Varecia were completely naı̈ve of the threat
posed by fossa making them particularly vulnerable to
Male 1
capture. None of these predation events has been wit-
Male 4
Female 1 nessed by MFG personnel.
Female 2
Female 3 3.4. Contribution to the wild population
Female 4
Female 5
Male 1 and female 1 reproduced in October 1998, but
Female 6
the infant(s) did not survive. The pair reproduced again
in October 1999, successfully raising triplets (two male,
one female) to beyond weaning (Britt et al., 2000b). To
date one of the triplets, a male is surviving. Male 2 has
integrated into a wild group. He is strongly suspected to
have sired a single infant with a wild female in October
2002. Female 6 was observed to mate with a wild male
in July 2002. In October, she produced twins which she
has successfully raised beyond weaning. Thus to date
matings between the released captive-bred Varecia
and the resident population have resulted in the birth
of three infants, all of which have survived beyond
weaning.
4. Discussion

3.3. Causes of death The results to date illustrate that there is no sig-
nificant difference in survival between animals with
The most common cause of death for the released early experience in a free-ranging situation and those
Varecia was predation by the fossa (Cryptoprocta without, between young animals and mature animals, or
 A. Britt et al. / Biological Conservation 115 (2003) 319–327 323

Table 4
Dates and causes of death for captive-bred Varecia following release to the wild at Betampona

Individual Set Release Date Date of death Cause of death Post release survival (months)

Male 1 1a/2b 10 November 1997 October 2000 Fossa 35

Female 1 1a/2b 10 November 1997 July 2000 Fossa 32
Female 2 1a/2b 10 November 1997 February 1998 Fossa 3
Male 3 1a/2a 10 November 1997 August 1998 Weight loss 8
Female 3 1a/2b 20 November 1998 February 1999 ? 3
Male 4 1b/2b 25 November 1998 November 2000 Fossa 23
Female 5 1b/2b 25 November 1998 June 2000 Fossa 19

between males and females. However, differences
between young and mature animals and males and
females in survival without supplementary feeding
approached significance. Young animals and males sur-
vived longer without supplementary feeding than
mature animals or females. These apparent differences
are likely to be an artefact of the small number of ani-
mals released.
It is difficult as yet to draw any firm conclusions from
this study as the statistical calculations are dependent
on the eventual fate of the five animals that are still
surviving and due to the low sample size of animals
released.
All Set 1a animals have been observed to have some
degree of contact with wild individuals. While the social
dynamics of Varecia appears to be variable between
populations (Morland, 1991; White, 1991; Balko, 1998),
at Betampona the species exists in loose communities
composed of relatively stable sub-groups (personal obser-
vation). As in the study by White et al. (1993) females
remain within their natal territory, and males disperse,
although not necessarily outside of their community.
Adult mortality of the released captive-bred Varecia
has been high (53.8%) (see Table 4) in comparison to
that recorded for the wild study group during the same
period (10%). Only one wild adult has apparently dis-
appeared since 1997. The major cause of death for the
released Varecia has been predation by the fossa (C.
ferox). To the best of our knowledge no adult wild
Varecia at Betampona have been taken by fossa during
the same period. It appears that captive-bred Varecia
are particularly vulnerable to predation. Four of the five
predation events occurred within a 6-month period
from June to November 2000. It is hypothesised that
one fossa began to specialise in Varecia during this per-
iod, perhaps having discovered that these naı̈ve animals
were relatively easy to capture in comparison with the
wild population. A similar phenomenon is reported by
Butynski et al. (1990) concerning the effect of one leo-
pard (Panthera pardus) on a population of Gorilla gor-
illa berengei. No further predation by fossa has occurred
since November 2000.
Could captive-bred Varecia be trained to avoid pre-
dation by fossa? One suggestion is that captive-bred
Varecia spend excessive time on the ground, making
them especially vulnerable to fossa predation. By hous-
ing small, muzzled dogs in the same enclosure to harass
the Varecia, ground use would be discouraged. How-
ever, fossa are excellent climbers and particularly skilled
at moving rapidly in an arboreal environment (Wright
et al., 1997). As none of the predation events has been
witnessed at Betampona, it is not known whether these
occurred on the ground or in the trees. The fact that 5
out of 13 Varecia fell victim to fossa predation suggests
that fear of this animal may not be innate in Varecia. It
can be concluded that avoidance of fossa is a learned
behaviour, i.e. infants learn from the example of their
parents. This is perhaps one reason to aim for rapid
integration of released animals into wild groups, in
order that they can learn from the example of their wild
conspecifics (see below).
The only other known cause of death is that of a
young group 1a male. He probably died as a result of
injuries sustained in a fall, but it is likely that the fall
was a result of his weak and malnourished condition.
This first alerted the monitoring team to the apparent
problems the released Varecia experience in maintaining
body weight during the austral winter. The male
weighed 2.1 kg when located. Shortly after another male
was found in a collapsed state, weighing 2.4 kg (mean
adult Varecia body weight typically falls within the
range of 3.0–3.5 kg). A non-invasive weighing system
has since been developed to monitor body weights
throughout the winter period. It is suspected that wild
Varecia experience similar weight loss during the winter
months. The causes of this weight loss are likely to be a
complex interaction of various factors, including
thermo-regulatory stress and reduced food availability
and quality. However, it is also likely that wild Varecia
are better able to cope with winter conditions through a
variety of adaptive behaviours and through information
learnt from parents and other group members.
This seasonal loss of condition provided justification
(with hindsight) for the ‘soft’ release strategy adopted at
Betampona. ‘Soft’ releases are financially more costly
than ‘hard’ releases, but in the long-term are more likely
to be successful (Cowlishaw and Dunbar, 2000). The
success of ‘soft’ releases can be improved by a training
324 A. Britt et al. / Biological Conservation 115 (2003) 319–327
or rehabilitation phase to encourage independence from
humans. Rehabilitation involves active coaching to
develop skills in foraging, antipredator and rearing
behaviour. Although not involving active coaching,
‘boot camp’ training at DUPC and St. Catherine’s
Island allowed the release candidates to experience tra-
velling using natural substrates, foraging for natural
food resources and the presence of potential predators
(e.g. raptor species). The rehabilitation phase of the
golden lion tamarin project systematically trained the
tamarins how to feed, avoid danger and locomote using
new substrates (Kleiman et al., 1986).
Many primate behaviours are learned and standard
learning periods may be many years in length. This
presents a particular problem for captive-bred animals
that have never experienced the wild (e.g. Yeager,
1997—orang-utans). The longest surviving Varecia
released at Betampona is a male who has integrated into
a wild group. Evidence suggests that it is male Varecia
who leave their natal territory and search out a new
group (White et al., 1993). Thus it would perhaps be a
preferable to release only young, sexually mature males
on the periphery of existing wild groups, in order to
increase the chances and rapidity of reproduction with
the existing population. It can be hypothesised that by
encouraging such rapid integration the released animals
will learn vital survival skills from their wild conspecifics.
The released Varecia were not from the same clade as
the Betampona population. It appears that the entire
captive population derives from the Ranomafana/Man-
ombo clade (Wyner et al., 1999). Hence the question of
the genetic compatibility of the stock released is raised.
One can argue that this may be beneficial for the
Betampona population through introducing new genetic
material. Equally there could be a risk of genetic pollu-
tion and outbreeding depression. There exists the poten-
tial for the loss through hybridisation of specific
adaptations to the local environment (Templeton, 1986),
e.g., seasonality and food resources. However, at
Betampona it was felt that the population was so small
that the risk of introducing animals that may not be
genetically compatible in order to save the population
was justified. Indeed, hybridisation of races within a
species may result in hybrid vigour (Wayne et al., 1994).
The dangers of disturbing the existing wild population
of Varecia at Betampona, e.g., through the introduction
of disease (Woodford and Rossiter, 1994; Cunningham,
1996), were considered. Even if, after the rigorous
veterinary screening of release candidates, a disease was
introduced to the Betampona Varecia, it would only
affect one small, isolated sub-population, and would
pose no threat to the metapopulation as a whole. What
could potentially be learned from the release was felt to
justify this small risk.
If the original cause of decline has not been removed
restocking or re-introductions should not proceed.
Although Varecia in general (and indeed the majority of
lemur species) are disappearing throughout Madagascar
because of competition with humans for space, at
Betampona this is not the case. The reserve has been in
existence since 1927 (Andriampianana and Peyrieras,
1972), and while the vast majority of the surrounding
forest has been cleared, the reserve has remained rela-
tively untouched. In recent times the main threat to the
Betampona Varecia has not been loss of habitat per se,
but small-scale hunting by local people. Evidence of this
was provided in the early 1990s by the discovery of
numerous snares and shotgun cartridges (personal
observation). The effects of the removal of even one or
two individuals from such a small population could be
significant. The presence of the MFG research team at
Betampona has acted as a significant deterrent to hunt-
ing. Thus it was felt that the immediate threat to the
Betampona Varecia could be controlled, if not removed
completely.
Can the Betampona project be judged a success?
Kleiman et al. (1991) suggest two differing measures of
success depending on the ecology of the species released.
For ‘K-selected’ species the simple post-release survival
of re-introduced individuals can be taken as an indica-
tion of success. However, for ‘r-selected’ species re-
introductions can only be regarded as successful if there
is reproductive output and infant survival during the
early years. Project Betampona adopted the criteria for
success suggested by Kleiman et al. (1991) for ‘r-selec-
ted’ species. In addition, given that the release pro-
gramme at Betampona aimed to reinforce the existing
wild Varecia population, further indicators of success
include integration into wild groups and reproduction
with wild individuals.
The survival rate to date at Betampona (38.5%)
compares very favourably with that achieved by the
golden lion tamarin release programme. In addition
successful integration and reproduction with the wild
population has occurred. This experiment has demon-
strated that captive-bred Varecia can survive and
reproduce in the wild, but is the release of captive-bred
animals the best means to reinforce an isolated popula-
tion? Data from translocations of wild primates
demonstrate that such approaches can succeed across a
range of primate ecological niches (Cowlishaw and
Dunbar, 2000). Re-introductions of captive-bred ani-
mals are very expensive. Kleiman et al. (1991) estimated
that each surviving golden lion tamarin re-introduced to
the wild cost $22,563. Is this a cost-effective use of con-
servation resources? There are two schools of thought.
First, there are those who consider that the money would
be better spent on in situ habitat protection (Mackinnon
and Mackinnon, 1991). The other school emphasises the
additional benefits which arise from re-introduction
programmes that make a significant contribution to
conservation (Stuart, 1991). The cost of releasing each
 A. Britt et al. / Biological Conservation 115 (2003) 319–327
Varecia in Betampona may be significant, but the spin-
off benefits for the conservation of all the flora and fauna
within the reserve must be considered. For example,
methods of captive propagation for indri (Indri indri) and
simpona (P. diadema diadema) are still to be developed,
and yet populations of these species at Betampona can
benefit from the increased protection of the reserve
afforded by the release programme for captive-bred
Varecia. Thus, captive-breeding is indirectly contribut-
ing to the conservation of these species.
Remember though that one aim of Project Betam-
pona was to reinforce the existing, isolated Varecia
population. This may have been better and less expen-
sively achieved by translocating animals locally from
‘doomed’ patches of forest, for example, the nearby
classified forest of Antanamalaza (Britt et al., 1999).
Primate translocations have a good potential as a con-
servation tool provided suitable habitat exists (Cow-
lishaw and Dunbar, 2000) and also have a higher
success rate than re-introductions of captive-bred ani-
mals (Griffith et al., 1989). However it is unlikely that
translocations would capture the public imagination or
attract sufficient funding in comparison to a far more
charismatic release of captive-bred animals to the wild.
Thus we face a dilemma, while translocations are more
likely to succeed, they are perhaps less likely to receive
funding, and while re-introductions are less likely to
succeed and may well be more expensive, they are more
likely to attract funding. Eight of the 10 primate trans-
locations reviewed by Cowlishaw and Dunbar (2000)
can be regarded as successful. Finally, a word of cau-
tion—it is important not to lose sight of perhaps the
most effective means of conservation—preserving habi-
tat and avoiding its fragmentation. The effects of a
restocking event were modelled for a metapopulation of
Cercopithecus mitis in Natal (Swart and Lawes, 1996).
While restocking improved the probability of persis-
tence in the short-term ( < 500 years), corridors were a
more effective management strategy for extending per-
sistence beyond 500 years. On this evidence we must
consider very carefully how best to make use of avail-
able funds for conservation.
Acknowledgements
Project Betampona would like to acknowlege Mada-
gascar’s Association Nationale pour la Gestion des
Aires Protégées (ANGAP), the Ministère des Eaux et
Fôrets and the Circonscription Scolaire de Toamasina-
II for their technical support and collaboration. We are
grateful for the continuing support and assistance of all
Madagascar Fauna Group (MFG) member institutions
who generously provide funds, equipment, technical
expertise and moral support for our work. We are
indebted to MFG Chief of Staff, Dr. Eva Sargent, for
325
her tremendous efforts on the project’s behalf. We
would like to specially thank staff of the San Francisco
Zoo, Durrell Wildlife Conservation Trust, Zoological
Society of London (ZSL), Marwell Zoo, Philadelphia
Zoo, St. Louis Zoo, Wildlife Conservation Society,
Zurich Zoo, Institute for the Conservation of Tropical
Environments, Duke University Primate Center and the
Friends of DUPC. This work would not have been
possible without generous grants from Mr. John Cleese,
the Margot Marsh Biodiversity Foundation, the Thelma
Doelger Charitable Trust, the American Zoological
Association Conservation Endowment Fund and the
Disney Wildlife Conservation Fund. A.B. would like to
personally thank Dr. Robin Crompton and Liverpool
University for providing him with an honorary research
fellowship and a work base in the UK. Thanks also to
Dr. Glyn Davies (ZSL), and Dr. David Britt for com-
menting on and suggesting improvements to the original
manuscript. Finally the greatest thanks must go to the
dedicated research team at Betampona, past and pre-
sent: Ianesy Fidel, Jean-Noel, Ramialison Shuman Eric,
Razafy Celestin, Razanadahy Arsene, Talata Pierre,
Tevomanana Guy Celestin, Tsirindahy, Georges and
Iambana Bernard Richardson—‘Misaotra betsaka
jiaby!’
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