178 THE DEVELOPING ZOO WORLD

REFERENCES ARNOTT, J., EMBURY, A. & PRENDERGAST, R. (1994): Pygmy HippopotaniusIMandrill exhibit at Mel- bourne Zoo. Int. Zoo Yb. 3 3 252-262. EMBURY, A. S. (1992): Gorilla Rainforest at Mel- bourne Zoo. Int. Zoo Yb. 31: 203-213. PUBLIC EDUCATION REVIEW GROUP (Unpublished): Melbourne Zoo themeslmessages: a way of developing

interpretive messages. The Royal Melbourne Zoolog- ical Gardens, 1993. VINCENT, E. & ASSOCIATES (UnpubIished): The Ro-va/ Melbourne Zoological Gardens graphics standards manual: a circulatory and information sign system for the Royal Melbourne Zoological Gardens. The Royal Melbourne Zoological Gardens, 1991.

Manuscript submitted 24 November 1993; revised 31 July 1995.

Int. Zoo Yb. (1995) 3 4 178-185 0 The Zoological Society of London

Three decades of Snow leopards

in captivity Panthera uncia

LEIF BLOMQVIST International Studbook Keeper and EEP Co-ordinator for Snow Leopards, Helsinki Zoo, Korkeasaari, FIN-00570 Helsinki, Finland

The international studbook for Snow leopards Panthera uncia was established at Helsinki Zoo in 1976. This paper reports on the status of the captive population over the last three decades and contains genetic and demographic analysis using the Single Population Analysis and Records Keeping System computer program. The number of collections main- taining the species has increased from ten in 1961 to 160 in 1991 and the captive population as at 1 Jan- uary 1992 was 541. A total of 1599 Snow leopards have been listed in the studbook of which 27% (428), one-third of wild-caught and a quarter of captive- bred animals, have bred. The captive population has 53 founders 11 of which are still living. Founder genetic contribution ranges from 0.1 to 8.6% with a mean representation of 1.8 1,95u/. As at January 1992 98% of the living population was captive bred.

Studbooks are an essential tool for the management of captive populations. The number of international studbooks has increased from nine in 1960 to 140 in 1993 (Olney, 1994). As more species become threatened in the wild a growing number of zoo collections are adopting a policy of maintaining rare animals in captivity (IUDZGICBSG (IUCNESC), 1993). This

ex situ management can support the con- servation of threatened species in the wild.

Although the first studbooks provided little more than a register for a particular species many have developed into sophis- ticated tools for population management and can be used to produce Master Plans to preserve the demographic and genetic health of a captive population.

The international studbook for the Snow leopard Panthera uncia was estab- lished at Helsinki Zoo in 1976 (Blomqvist, 1978a) and has been published regularly by the author ever since. By the mid-1970s the number of collections housing Snow leopards had increased and an inter- national studbook was considered urgent. Between 1992 and 1993 the studbook data was entered into the Single Population Analysis and Records Keeping System computer program developed by ISIS (Scobie, 1993) to increase uniformity among studbook keeping systems. Because data on Snow leopards main- tained in Chinese Zoos are only available

REVIEW SNOW LEOPARDS IN CAPTIVITY 179

REGION %, POPULATION AS AT 1 JAN 1992

North America 54 Europe 34 Japan 6 Russia/ Kazakhstan 4 Asia 1 Oceania 1

Table 1. Regional distribution of the captive Snow leo- pard Panthera uncia population as at 1 January 1992.

from 1986 the Chinese captive population has been excluded from this report. After the Seventh International Snow Leopard Symposium was arranged in Xining in 1992, it was agreed that Mr Lu Xiandong from Tianjin Zoo will serve as the regional species co-ordiiator for China.

STATUS OF THE CAPTIVE POPULATION AS AT I JANUARY 1992 Since the first edition of the International Pedigree Book for Snow leopards in 1976 (Blomqvist, 1978b) 769.735.95 Snow leo- pards from over 30 countries and six geo- graphic regions have been listed (Table 1). The number of collections holding the species has increased from ten in 1961 to 160 in 1991. As at 1 January 1992 there were 541 Snow leopards in captivity, of which 5.7 (2%) were wild-caught and the remaining 270.259 captive bred.

During 1991, 40.35.4 cubs were born in 37 litters. Evansville had one litter of

no. animals 600 500

300

quadruplets of which three survived. Infant mortality in 1991 was 27% (9.8.4) and a further 18.22 subadult/adult Snow leopards died during the year. There were no importations from the wild during 1991 thus the total population on 1 Jan- uary 1992 was 215.266, an increase c. 3% from the previous year (Blomqvist, 1993).

STATUS OF THE CAPTIVE POPULATION

Although Snow leopards were exhibited in zoos at the turn of the century only 58.59.13 and 13 litters were recorded for the period up to 1961. Because of this small population size only animals listed since 1961 are included in this report. There was little breeding during the 1960s and the captive population was dependent on importation of wild-caught animals. In the early 1970s captive breeding had increased and by 1974 the number of cap- tive-bred Snow leopards exceeded wild- caught animals for the first time (Fig. 1).

Although the number of Snow leopards born in captivity was growing the species was still considered difficult to breed; cubs were often rejected and the number suc- cessfully hand-reared was extremely low and mortality in mother-reared cubs was high. Adults often died because of impaired resistance to diseases not found in their natural high-altitude habitats.

A growing concern for the species in the wild, and low reproduction and high mor- tality in captivity prompted three Euro-

1961-1 991

200 100 0 1961 1966 1971 1976 1981 1986 1991

Fig. 1. Ratio of captive-bred (white) and wild-caught (black) Snow leopards Panthera uncia in captivity between 1961 and 1991.

180 THE DEVELOPING ZOO WORLD

3 d i'v LINK TOTAL

Total registered Wild caught Captive bred

Alive at 1 Jan 1992 Wild caught Captive bred

BREEDING ANIMALS Total number that have bred Wild caught that have bred Captive bred that have bred

Total breeding animals alive as at I Jan 1992 Wild caught Captive bred

769 735 95 148 146 I I 62 1 589 84

215 266 5 I

270 259

214 214 48 50

166 164

I29 I34 5 6

123 I29

I599 305

I294

54 1 12

529

428 98

330

263 11

252

Table 2. The status of the captive Snow leopard as at 1 January 1992.

pean zoo directors, Peter Weilenmann (Zurich), Walter Encke (Krefeld) and Ilkka Koivisto (Helsinki) to organize the first International Snow Leopard Sym- posium, held at Helsinki Zoo in March 1978 (Blomqvist, 1978~). The symposium focused on captive breeding and increasing scientific and public awareness of this highly endangered felid. Sub- sequent conferences were held at Zurich, Seattle and Krefeld. In 1986, the Fifth International Snow Leopard Symposium was arranged in Srinagar, India (Freeman, 1988). This was the first to be held in a country with indigenous popu- lations of Snow leopard.

By the mid-1980s captive management of Snow leopards had improved and cap- tive breeding increased, particularly in North America but also in western Europe. Wild populations were given the highest conservation priority and in 1981 the International Snow Leopard Trust was founded by Helen Freeman in Seattle to increase world-wide public awareness of the importance and fragility of moun- tain habitats and the conservation of animal species endemic to them. In addi- tion the ISLT has successfully undertaken the challenging task of co-sponsoring the

Symposia which, after Srinagar, were arranged in Alma-Ata, Kazakhstan, in 1989 (Blomqvist, 1990), and Xining, Peo- ple's Republic of China, in 1992 (Fox & Jizeng, 1994).

REPRODUCTION The status of the captive population as at 1 January 1992 is shown in Table2. Of the 1599 animals listed in the studbook 27% (214.214) have bred. To date, one third of wild-caught and a quarter of cap- tive-bred animals have bred. Ninety-eight per cent of the living population are cap- tive-bred (Fig. 1) and 36% of these are either too young to breed or have been prevented from breeding in order to find a compromise between maintaining the largest genetically viable population possible and allocation of limited space and resources to endangered taxa.

Both sexes are sexually mature at three years of age. Seven per cent of 09 con- tinue to breed until the age of 15 years and 4% of 66 continue to sire until the age of 17 years. Most successful mating occurs between the ages of four and 11 years old. A total of 1221 births to par- ents of known age are shown in the

REVIEW: SNOW LEOPARDS IN CAPTIVITY 181

fecundity sol

age (years)

Fig. 2. Fecundity curves for J (solid line) and 9 (bro- ken line) Snow leopards; 1121 birth events to parents of known age are recorded.

mortality 701

30 20

J

2 4 6 8 10 12 14 16 18 20 22 age (years)

Fig. 3. Mortality curves for 3 (solid line) and 9 (bro- ken line) Snow leopards of known age (n=820 deaths).

fecundity curves (Fig. 2: curves have been smoothed).

MORTALITY The mortality curves for 870 animals of known age can be seen in Fig. 3 (curves have been smoothed). Thirty-day mor- tality between 1961 and 1991 is shown in Fig. 4. Over the last 30 years a mean 38% of cubs have died within their first year.

Mortality values for cubs in the early 1960s (100% in 1961 and 1963) are the result of low sample size and therefore warrant less confidence. From the mid- 1970s the number of cubs bred in captivity is fairly high and the values are more significant (Fig. 4). Although 30 day mor- tality is decreasing it was still between 20 and 30% in 1989-1991. After the age of 14 years 9 mortality increases rapidly; males tend to live longer with a higher mortality after the age of 17 years. The longest recorded life span for a Snow leo- pard in captivity is 21 years.

DEMOGRAPHIC ANALYSIS An evaluation of the demographic status requires knowledge of the age and sex structure of the population, the age at death and the age of breeding 99 (fecundity). The sex and age structure of the captive Snow leopard population from 1962 to 1 January 1992 is shown in Fig. 5. Age distribution consists of living 66 and 99 per age class. The shape of the age pyr- amid indicates whether a population is stable, growing or decreasing. In a stable population more animals are found in the younger classes and there is a steady decline in the older age classes. In 1962 (Fig. 5a) all age classes were under repre- sented and without the importation of wild-caught animals this population could have become extinct in captivity. By 1972, as a result of importation (mainly from the former Soviet Union), the population had increased 216% (from 37 to 117)

% mortalitv

l " " I " " l " " l " " I " ~ ~ I 1961 1966 1971 1976 1981 1986 1991

Fig. 4. Percentage of 30 day mortality in Snow leopard cubs bred in captivity between 1961 and 1991.

182 THE DEVELOPING ZOO WORLD

Fig. 5. Age structure of the Snow leopard population as at: a. 1 January 1962; b. 1 January 1972; c. 1 January 1982; d. 1 January 1992.

(Fig. 5b). An increase in captive breeding can be seen in the pyramid for 1982 and the number of young animals (1-3 years) exceeds animals in the older age groups (Fig. 5c). As mortality levels are high it is unlikely that all of the younger animals will reproduce but good population growth can be predicted. Figure 5d shows age and sex distribution as at 1 January 1992. It can be seen in the 0-2 age classes that the breeding restrictions recom- mended by the regional breeding pro- grammes are starting to be effective. Almost 46% (251) of captive Snow leo- pards are within the prime breeding-age bracket of four to 11 years old, 45% (246 animals) are younger than four years and 9% (49 animals) are older than 11 years and will soon stop breeding.

One measure of the efficacy of genetic management of a captive population is the effective population size N,. This is a measure of the genetic variation present in

a population which is transmitted from one generation to the next. As at 1 Jan- uary 1992, 263 animals were proven breeders (Table 2). This number permits the computation of the effective breeding size for the 1991 population using the for- mula: N, = (4 x M x F) - (M+F) = 263, where M is the number of breeding 88 and F the number of breeding 99. N, is equivalent to 49% of the total captive population.

A summary of fluctuations in the cap- tive population owing to importation from the wild, births and deaths can be seen in Fig. 6. Between 1981 and 1991 only 14 wild-caught Snow leopards were brought into captivity. Despite improved management the total mortality is still high averaging c. 29% over the last 30 years. The 18.22 subadult/adult deaths have resulted in a high mortality value for 1991.

REVIEW: SNOW LEOPARDS IN CAPTIVITY 183

FOUNDER REPRESENTATION A founder is defined as an individual with no known genetic relationship to any animal in the pedigree except for its own descendants. Wild-caught animals without living descendants are potential founders and only become actual founders once they produce offspring. For a captive population it is desirable to have as many founders as possible. Although a pair of individuals contain an average of 75% of the heterozygosity for quantitative traits in the source population, rare alleles will not survive such a small bottle-neck in the number of founders (Soul6 et al., 1986). To achieve adequate representation of a wild population approximately 20 foun- ders are recommended (Soul6 et al., 1986). If selected randomly from the wild, these 20 founders would contain nearly 98% of the genetic variability present in the wild population (Lacy, 1989).

Established breeding programmes exhibit a wide range of founders: Bara- singah deer Cervus duvauceli, n = 3 (Foose et al., 1986); Golden lion tamarin Leonto- pithecus r. rosalia, n=44 (Foose et al., 1986); Przewalski horse Equus przewalskii, n = 13 (Ryder & Wedemeyer, 1982); Wol- verine Gulo g. gulo, n = 11 (Blomqvist, 1994); Amur tiger Panthera tigris altaica, n = 68 (Christie, 1994a); Sumatran tiger Panthera t. sumatrae, n= 17 in Europe (Christie, 1994b); Cheetah Acinonyx jub-

atus, n = 72 (Marker-Kraus & Grisham, 1993). The 1991 Snow leopard population was descended from 53 actual founders. Of the 305 wild-caught individuals main- tained in captivity since the last century 68% (207) have died without contributing to the present gene pool (Table 2). Ten founders are still alive and there is one potential founder, a wild-caught animal which has not bred.

Equal founder representation in the descendant generation assures that genetic variants present in each founder are not excluded from the descendant population while other founder alleles are present in many copies (Lacy, 1989). A descendant population with unequal founder repre- sentation will contain less genetic vari- ability than a population based on the same number of founders in which there has been equal representation. The founder contribution in the Snow leopard population varies from 0.1 to 8.6%. Given 53 actual founders the contribution of each animal should be 1.8%. Founder rep- resentation as at 1 January 1992 was 1.8 & 1.95% with ten founders (18.5%) having contributions outside the range (Fig. 7).

DISCUSSION The survival of Snow leopards and other large felids may increasingly depend on wild population management and e x situ

no. animals 120- 100- 80- 60. 40-

Fig. 6. Births (solid line), deaths (broken line) and transfers from the wild (dotted line) in the captive Snow leopard population between 1961 and 1991, also showing the reduction in the number of births between 1989 and 1991 which is the result of breeding restrictions.

184 THE DEVELOPING ZOO WORLD

founders (stdbk no.) Fig. 7. Founder representation in the global captive Snow leopard population as at 1 January 1992 (parity = 1.8%).

captive-breeding programmes. Wild popu- lations are under pressure and the Snow leopard is classified as Endangered throughout its range by the IUCN and listed in Appendix I (i.e. most in need of protection) by CITES. At time of writing the wild population may consist of several thousand individuals; a number that does not suggest immediate extinction. The Snow leopard is protected in most of the countries within its native range but retal- iation against livestock losses and demand for Snow leopard products, such as bones for medical purposes, continues to threaten wild populations and we cannot afford to be complacent about the future. If persecution of the Snow leopard could be brought under control wild popu- lations may have the opportunity to recover to more secure numbers; however, many local populations are fragmented and are possibly non-viable either geneti- cally or demographically. Panthera uncia is one of the few large felids which has vast areas of rugged habitat unsuitable for human settlement. In the future it might be possible for animals from the captive population to restock these fragmented wild populations.

The Snow leopard has been the subject of intense conservation with an inter- national studbook since 1976 and regional breeding programmes in North America (SSP), Europe (EEP), Japan (SSCJ), Aus- tralasia (ASMP) and Russia. All regional breeding programmes are co-ordinated by the International Studbook Keeper and have a species co-ordinator and a species committee elected by the participating zoos. Their goal is to maintain stable and self-sustaining populations in both number of animals and genetic variation. It is possible to assign each Snow leopard a target level of representation in the global management plan. Population geneticists have recommended an effective population size of 250-500 as the absolute minimum for preservation without steady loss of genetic variability (Frankel & Soulk, 1981; Soule, 1983). With an inter- national captive population of 541 animals as at 1 January 1992 the Snow leopard is within this recommendation. Mortality in captivity is still relatively high and poaching, disease, starvation and competition reduce numbers in the wild. Successful breeding programmes have a potential to produce a surplus and

REVIEW. SNOW LEOPARDS IN CAPTIVITY 185

some animals may have to be prevented from breeding if target levels of represen- tation are to be achieved. A breeding pro- gramme does not always mean breeding but can often mean not breeding. Captive populations must be managed to establish an effective population size sufficient to allow replacement by new mutation of diversity at a rate equal to the loss of diversity by genetic drift and inbreeding (Seal & Foose, 1983).

Keeping endangered populations nu- merically sound by increasing longevity and reproduction is not sufficient to ensure species survival. The quality of each captive population is as important as the quantity and genetic degeneration and unfavourable selection must be avoided.

Captive-breeding programmes demon- strate to zoo visitors that we are com- mitted to helping conserve threatened species. The Snow leopard is a perfect example of a flagship species which can highlight the fragility of mountain habi- tats. We have to explain that conservation of the Snow leopard only makes sense if we also attempt to preserve the natural habitat for possible future reintroduction. The international captive-breeding pro- gramme for the Snow leopard can and has to serve as a publicity nucleus for the con- servation of the whole mountain biotope and the hundreds of less conspicuous species which share the same habitat.

REFERENCES BLOMQVIST, L. (1978a): First report on the snow leo- pard studbook Pantheru uncia and 1976 world reg- ister. Int, Zoo Yh. 18: 227-231. BLOMQVIST, L. (1978b): Snow leopard register 1. In Internutional pedigree book of snow leopards Panthera uncie I: 131-140. Helsinki: Helsinki Zoo. BLOMQVIST, L. (1978~): First international snow leo- pard conference in Helsinki, 7th-8th March 1978. Int. Zoo News 25(5): 5-6. BLOMQVIST, L. (Ed.) (1990): International pedigree book of snow leopards. 6. Proceedings of sixth inter- national snow leopard symposium in Alma-Ata 1989. Helsinki: Helsinki Zoo. BLOMQVIST, L. (1993): The snow leopard in captivity in 1990. In The Nordic Ark, Annual Report 1992:

2043. Hunnebostrand: The Nordic Ark/The Bohus Breeding Centre Trust. BLoMQVIST, L. (1994): Regiond studbook ,for wol- verine Guio g. gulo 1. Hunnebostrand: The Nordic Ark/The Bohus Breeding Centre Trust. CHRISTIE, S. (1994a): Europetrn siiidbook f o r the Amur tiger Panthera tigtis altaica 1. London: The Zoological Society of London. CHRISTIE, S. (1 994b): European studbook for the Sumatran tiger Pantheva tigris sumatrae 3. London: The Zoological Society of London. FOOSE, T. J., LANDE, R., FLESNESS, N. R., RABR, G. & READ, B. (1986): Propagation plans. Zoo B i d 5 139-146. Fox, J. L. & JIZENG, D. (Eds) (1994): Proceedings qf the seventh international snow leopard xyniposium in Xining 1992. Seattle: International Snow Leopard Trust and Chicago: Chicago Zoological Society. FRANKEL, 0. H. & SOCJLE, M. E. (1981): Conserva- tion and evolution. New York: Cambridge University Press. FREEMAN, H. (Ed.) (1988): Proceedings oj' rhe j i f fh international snow leopard symposium. Bombay: International Snow Leopard Trust and Wildlife Institute of India. IUDZGlCBSG (ILJCN/SSC) (1993): The world zoo conservation strategy: the role of the zoos and aquuria of' the world in global conservation. Apple Valley, MN: CBSG. LACY, R. (1989): Analysis of founder representations in pedigrees: founder equivalents and founder genome equivalents. Zoo Biol. 8: 11 I--123. MARKER-KRAUS, L. & GRISHAM, J. (1993): Captive breeding of cheetahs in North American zoos:

OLNEY, P. (1994): Annual report on international studbooks and registers. CBSG News. 5(2): 25. RYDER, 0. A. & WEDEMEYER, E. A. (1982): A co- operative breeding programme for the Mongolian wild horse Equus przewalski in the United States. Biol. Conserv. 2 2 259-272. SCOBIE, P. N. (1993): Single population analysis and records keeping system (SPARKS) , version 1.11. 20 April 1993. Apple Valley, MN: ISIS. SEAL, U. S. & FOOSE, T. (1983): Species survival plan for Siberian tigers in North American zoos: a strategy for survival. AAZPA a. Conf: Proc. 1983 3340. SOULE, M. E. (1983): What do we really know about extinction? In Genetics and conservafion. Schone- wald-Cox, C., Chambers, S. M., MacBryde, B. & Thomas, W. L. (Eds). Reading, MA: Addison- Wesley Publishing Co. SOULE, M. E., GILPIN, M., CONWAY, W. & FOOSE, T. J. (1986): The millennium ark: how long a voyage, how many staterooms, how many passengers? Zoo Biol. 5 101-113.

1987-1991. ZOO Biol. 12: 5-18.

Manuscript submitted 18 July 1994