zoolo,giral Journal uJflhr Lirrnean Societv ( 1989),95: 109-1 16. LVith 2 figures
The application of reproductive technology to
endangered species breeding programmes
GEORGINA M. MACE
Institute of ~ o o l o g y ,The zoological Society of London, Regent's Park,
London NW14KT
-
~
Captive breeding plays an increasingly important role in species conservation, hut special problems
are encountered in achieving the ideal of a demographically stable but genetically diverse population.
Breeding programmes involving co-operation among a number of crntres are now being developed
which will overcome some of these difiiculties by identifying individual animals, genetic lineages or
age cohorts from which to breed. Application of techniques such as artificial insemination, embryo
transfer and semen collection and storage, as well as the monitoring of reproductive status will
contribute to the success of such programmes. T h e usefulness of these procedures for various
population problems is discussed and criteria for their appropriate implementation within breeding
programmes is outlined.
KEY WORDS: -Conservation
- captive
breeding
~
grnctic m a n a g e m e ' n l ~reproductive
~
terhnology.
CON'I'EN'I'S
. . . . . . .
Introduction .
Captive populations as biological populations
Demographic management
. . . .
Genetic management . . . . . .
Founder effects .
. . . . .
Gcneration length
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.
Population managemrnt .
. . .
Management of population subunits
. .
Conclusions .
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Acknowledgements
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References
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INTRODUCTION
For an increasing number of species, captive breeding plays a n important role
in conservation, either by providing individuals for release or reintroduction, or
by maintaining stocks as insurance against the total loss of the wild population.
Breeding programmes are designed to maximize prospects for the survival of a
species over the long term, while also recognizing that resources are limited and
may need to be allocated to an increasing number of species (Foose, 1983;
Conway, 1986). This paper concentrates on the ways in which reproductive
technology, and especially the management of individual animal fertility, is
0024-4082/89/020109
+ 08 S03.00jO
109
1989 T h e Linnean Society of London
I10
G. M. MACE
important for the successful implementation of breeding programmes for rare and
endangered species.
To be effective in this conservation role, captive populations need to be
managed, with many different institutions co-operating in the best interest of the
species. The kind of management required is different from that regularly
practised either by agriculturists with domesticated species or by wildlife
managers with wild reserves. T h e aim is not to domesticate the species or even to
select for any particular trait, as future environments may well be different from
a n y to which it could now be adapted by selective breeding. Unless there are
clearly detrimental genetic traits in the population, the aim should be to preserve
a maximum level of genetic variation and to avoid selection (Frankham et al.,
1986). The population also needs to be managed for a stable size and structure.
This will provide overall stability and reduce extinction risks as well as being
amenable to manipulation to provide excess for reintroduction or release, as and
when required. Stable populations are less susceptible to extinction pressures and
also retain more genetic variation than fluctuating populations of similar size.
The overall goals of most captive breeding programmes are therefore to sustain
genetically diverse and demographically stable captive populations.
CAPTIVE POPULAI’IONS AS BIOLOGICAL POPULATIONS
Management regimes for captive populations are based on techniques from
standard population biology developed for studying populations in the wild.
Captive populations may differ from wild populations in several ways. First, most
individuals are maintained in zoos or similar facilities where, at least for larger
forms, the number in any one collection is relatively small. Even within national
boundaries or quarantine zones the number is low with very little immigration or
cmigration. Therefore, the basic population unit is usually small and closed.
Secondly, for many rare and endangered species the animals now in captivity are
several generations removed from their wild ancestors. With no prospect of more
wild-born animals, the manager may be faced with a population already in some
kind of genetic or demographic crisis. Although both genetically and
dcmographically captive populations differ from natural populations, many of
the standard techniques can still be usefully applied, both to assess status and
suggest methods for improved population management. I n fact, as habitat loss
causes wild populations to become increasingly fragmented, they will also come to
facc similar problems to captive populations. T h e experience of managing captive
populations should therefore also lead to the development of effective techniques
for managing endangered species in their natural habitats.
DEMOGRAPHIC MANAGEM EN’I
A basic problem is posed by captive populations that are declining in numbers.
For example, the age structure of the captive population of the highly endangered
black rhinoceros (Diceros bicornis) is heavily biased towards animals aged 10-20
years with few younger individuals to form the breeding core in a few years time.
A recent analysis of studbook data (Lindemann, 1984) suggests that the captive
population may decline by about 5001, over the next ten years. There are several
contributory factors, but one is that almost 40% ofadult females are not breeding.
ENDANGERED SPECIES BREEDING
111
Identification of relevant females, investigation into their physiological status,
and some appropriate therapy could rapidly improve the situation.
A more common problem is a population that is expanding rapidly. For many
species, captive breeding is highly successful and populations seem likely to
swamp available resources within the next few generations (e.g. Siberian tigers,
Panthera tigris altaica, Seal & Foose, 1983; Przewalski horse, Equus przewalski,
Foose, 1980). Using standard demographic techniques based on life table
analysis, i t is possible to determine rates of fertility and survivorship that will
maintain population size at carrying capacity (Foose, 1980; Seal & Foose, 1983).
Reliable reversible contraceptive methods are required if these plans are to be
applied successfully.
A related problem is the unstable nature of many captive populations. For
example, the western lowland gorilla (Gorilla g. gorilla) population has been
increasingly dependent on captive breeding since the 1960-1970s when the last
wild-born individuals were imported, and the rather poor success up until the last
few years is reflected in the relatively small number of individuals in the
10-15 year age classes (Fig. 1 ) (Mace, 1988b). Such transitional events in
5
Number
.Wild born
UCaptive born
Figure 1. T h e age and sex structure of the world population of western lowland gorillas (Gorillag.
gorilla). Since the early 1970s few wild-born animals have been imported, and the population has
become dependent on captive breeding. T h e age strurture of the population is unstahle because
breeding succrss was initially piiiir (E'rum Maw, 1988h).
112
G M MACE
captive populations inevitably lead to unpredictable and fluctuating numbers
which are not suitable for management. Similar problems can arise from poor
population management of species which continue to breed well in captivity. This
can lead not only to fluctuating numbers with the concomitant risk of extinction,
hut also to poor genetic management, since periodically the population is
rrpopulated with young from a limited genetic background. Population
management can buffer the population by selection of particular individuals from
particular agc classes for breeding, but again successful implementation of the
programme depends on controlled breeding and controlled contraception.
Finally, because most captive populations are relatively small, they are
especially prone to stochastic processes which, by definition, defy prcdiction. Such
events can have a major impact on the viability of a population. For example, ten
male calves were produced consecutively in the re-introduced herd of Arabian
oryx in Oman (Stanley-Price, personal communication), giving cause for concern
about the longer term viability of the population of 30 animals. A couple of years
of poor breeding success in a population with rather high turnover can have a
similarly destabilizing effect. By their nature, these events are unpredictable, but
managers need to be able to respond appropriately, and this will often entail some
kind of managed breeding for a period to stabilize the population.
GENETIC MANAGEMEN’I’
Small populations that are maintained over a number of generations lose a
substantial proportion of genetic variation, and, largely by genetic drift and
selection, the genetic structure of the population will change, homozygosity will
increase and inbrecding depression may become significant (Frankel & Soule,
1981). In general terms, the larger the population size that can be maintained the
better. In practical terms reSources, especially for larger animals, are limited and
responsible management of one species should not deprive others (Foosc, 1983). If
the precise goals of the captive breeding programme are decided then a required
population size, often termed the ‘carrying capacity’, can be calculated (Soul6
el al., 1986). For example, a world population of 400 450 has been set for goldenlion tamarins (Lconlopilhecus rosalia) (Ballou, 1986), and 250 for Siberian tigcr in
North America (Seal & Foose, 1983).
l h e r e are three particular ways in which population management can
contribute to genetic management: by managing founder individuals, generation
length or the distribution of breeding within the population. These are discussed
below.
Founder efects
Clearly, the carrying capacity established for a species may be greater than the
actual number of wild-born individuals from which the population was founded.
The first generation in captivity can be a very significant stage for a captive
population. In many species, less than 50% of the wild-born founders have
actually bred, and this represents an enormous loss of population genetic
variation (Mace, 1986). Efforts spent to assess the status ofnon-breeding animals
and to manage their breeding subsequently (Hodges, 1985) will be well worth
r .
ENDANGERED SPECIES BREEDING
113
while. Failing this, the negative effects of small founder population sizes can be
reduced if the population is rapidly increased from founder number to carrying
capacity, ideally within one generation (Soule et al., 1986). Clearly, techniques
that can facilitate large numbers of offspring from each pair, including
interspecific embryo transfer, are appropriate here. For some species, several
generations of captive breeding are already passed, and Ballou (1984) has
discussed ways in which semen storage can be used to minimize founder effects in
complex pedigrees.
Generation length
Genetic variation is lost with each generation, so that over a fixed time interval
one effective means of maintaining variation is to increase generation length. This
can be achieved by breeding from older individuals, or, at least, by preventing
young individuals from breeding. This may need to be carefully managed as the
oldest individuals may be less fecund. There is some concern about neonatal sex
ratios in captive gorillas where older females apparently produce a greater
proportion of male offspring (Mace, 1988b). Mechanisms and adaptive
explanations for sex ratio distortion for other mammalian species have been
discussed recently (Clutton-Brock & Iason, 1986; Gosling, 1989) and the causal
factors for captive gorillas are still being investigated. However i t seems likely that
potentially damaging consequences can be avoided by prudent management.
The ultimate solution to loss of genetic variation is the long term storage of
gametes or embryos which reduces generation number to one, regardless of the
time scale. So far, however, reliable methods are available for only a few species
(Moore, 1985; Summers, 1986). Using semen collection and preservation it will
still be necessary to manage the population both to ensure sufficient females and
to minimize genetic divergence in the female line which might be detrimental
when the stored semen was used to fertilize the females after a number of
generations. In contrast, embryo storage provides long term preservation of
genetic material without the necessity for a living population, except to provide
suitable recipient females.
Population management
The extent to which genetic variation is retained in a population is influenced
by its size and by the way in which breeding success is distributed among
individual animals. The genetically-effective population size will be less than the
census number if the sex ratio among breeders departs from unity or if family size
varies widely among individuals (Frankel & Soulk, 1981; Crow & Kimura,
1970). These are common features of many polygynous species where, especially
in captivity, a few males may dominate breeding over long periods of time (Mace,
1986). Frequent changes of breeding males can increase the effective population
size in such cases, but may also be highly disruptive to the herd, and therefore to
breeding success. One solution to this dilemma is to impregnate females in
breeding herds with semen from different males. This would lead to a dramatic
reduction in family size variation, and therefore increase the genetically effective
population size. Similarly, in species such as some marmosets, where subordinate
females within social groups are reproductively suppressed (Abbott, 1987),
G. M . MACE
1 I4
genetic variation in the population could be maximized by endrocrine therapy
allowing subordinate females to reproduce normally.
Pedigree analysis of captive populations can also help identify key genetic
lineages in the population (MacLuer et al., 1986), and therefore the individuals
which should be given high priority as breeders (Mace, 1988a).Assessment of the
reproductive status of these individuals (Hodges, 1985) can promote breeding
success, and artificial insemination, or embryo transfer may then enable large
numbers of offspring to be produced by an individual, thereby safeguarding those
genes in the population. These techniques can also lead to identification of
individuals that are genetically surplus to the managed population, and to whom
contraception should be applied.
Finally in many species inbreeding has been shown to adversely affect rates of
juvenile survival (Ralls, Brugger & Ballou, 1979) (Fig. 2), but artificial breeding
techniques may help by facilitating the introduction of unrelated individuals to
the population. I n some cases it becomes hard to avoid inbreeding, but
reproductive management may then help to keep levels of inbreeding at a low
level, where it may be less detrimental (Fig. 2).
MANAGEMENT OF POPULATION SUBUNITS
Quarantine and health restrictions, as well as geopolitical boundaries and
economic considerations constrain movements of individual animals between
different sub-populations. T h e extent to which managed populations should be
sub-divided and the degree of migration between sub-units that is desirable varies
according to the circumstances relating to each species (Foose et al., 1986; Princee,
in press). However, most authors agree that sub-division with some migration is
optimal (Chesser, 1983; Lacy, 1987) and transfer ofgametes or embryos would be
cheaper, possibly easier from a health viewpoint, and certainly less disruptive to
individual animals, than will be transfer of the animals themselves.
-0
0.8 -
, 0.7-
.-
0.6-
30 days
u)
0-5>
c 0.4-
V
W
3
w 0.3-
E
3 months
I year
0.2-
O-'
O
O
0.06
-0425
0-156
-0.250
0-313
-0.375
Inbreeding coefficient
Figure 2. The relationship between inbreeding and survival in scimitar-horned oryx ( O y lno) born in
Britain between 1974 and 1986. Survival rates are significantly reduced at inbreeding levels above
0.125. Samples sizes are as follows: 0 (102), 0.06-0.125 (34),
0 . 1 5 6 4 . 2 5 0 (58), 0.313-0.375 (12).
ENDANGERED SPECIES BREEDING
1 I5
CONCLUSIONS
The value of captive breeding for conservation of species will depend on the
efficient management of populations from genetic and demographic standpoints.
Appropriate application of reproductive techniques such as semen collection,
artificial insemination, gamete and embryo collection and storage and embryo
transfer will not only help the aims of the breeding programme to be achieved,
but also will help to avoid disruption to individual animals.
ACKNOWLEDGEMENTS
I am grateful to Drs P. Bennett and A. Flint for commenting on an earlier
version of this manuscript, and to participants in the joint Zoological Society of
London and Linnean Society meeting for useful discussion.
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