Minimizing extinction probability due to demographic stochasticity in a reintroduced herd of Persian fallow deer Dama dama mesopotamica

Biological Conservation 75 (1996) 27-33 © 1995 Elsevier Science Limited Printed in Great BritairL All rights reserved 0006-3207/96/$15.00+.00

ELSEVIER

0006-3207(95)0004

1 -0

MINIMIZING EXTINCTION PROBABILITY DUE TO DEMOGRAPHIC STOCHASTICITY IN A REINTRODUCED HERD OF PERSIAN FALLOW DEER Dama dama mesopotamica David Saltz Nature Reserves Authority, 78 Yirmeyahu St, Jerusalem, 94467, Israel (Received 31 August 1994; revised version received 7 February 1995; accepted 14 February 1995) thought to be extinct throughout its range (Chapman & Chapman, 1980). In 1956, however, a remnant population of about two dozen animals was found along the Dez and Karkeh rivers in Kuzistan Province, Iran (Pepper, 1974). A world breeding programme was started at the Opel Zoo, Kronberg, with two males and a female (2,1) (Jantschke, 1991). The world studbook (Rudloff, 1991-93) lists a total of 57 (32,25) Persian fallow deer living in zoos, the majority of which are in the Berlin and Kronberg Zoos. There are approximately 250 animals in Iran, of which no more than 15 still exist in the wild (Heidemann, 1994), with the remainder in various captive herds. However, the future of the herds in Iran is uncertain due to poor management, lack of planning (Heidemann, 1994), and possible continued poaching (Reed, 1965). The Hai-Bar Carmel in Israel is a facility devoted to the propagation and possible reintroduction of species that were abundant in Israel in the past and were extirpated. The Persian fallow deer breeding core at HaiBar Carmel was founded from four (2,2) animals received from the Opel Zoo in 1976 (Jantschke, 1991). One of the females died shortly after arrival, but in 1978 four more females were received from Semeshkandeh reserve in lran. In 1979 there were nine (2,7) adults at Hai-Bar Carmel, and the herd steadily grew (Fig. 1) with a mean annual reproductive success (RS) of 0.78 fawns/doe/year (mean of annual reproductive success was weighted by the number of adult does in each year). Currently the herd stands at 96 adults (45,51) and 25 fawns (gender yet to be determined). A simple growth model assuming an exponential growth curve predicts a doubling time of less than 5 years. Thus, the herd is probably large enough now to support a reintroduction. The age structure and size of a reintroduced herd that will produce a given survival probability over a specified time period vary with the dynamics of the species. Consequently, various sizes and age structures of reintroduced herds must be evaluated separately for each species using available data on its life history. Extinction probability (EP) can be estimated through the use of computer simulations. The results enable identification of the age structure that will produce the lowest EP, and will also evaluate how sensitive the EP

Abstract The Persian fallow deer Dama dama mesopotamica is extremely rare in the wild, but reintroduction of breeding animals from the Hai-Bar Carmel, Israel, may be feasible. A life table was constructed from data available in the world studbook. I used a Monte Carlo Leslie matrix simulation model to estimate probability of extinction due to demographic stochasticity, using different female age structures and numbers of individuals. Based on the simulations, 13 prime-aged females aged 2-4 years would be required to ensure an extinction probability of less than 1% over the next 100 years. Substituting older age groups increases extinction probability, thereby increasing the number of animals needed to achieve a 0.01 extinction probability. Due to poor reproductive success at the Hai-Bar Carmel prior to 1990, few females older than 5 are available. Also, there are no more than 11 females in each of the 2-4 years age groups. Thus a combination of eight 2-year-old and five 3-year-old females or seven 2-year-old, four 3-year-old, and two 4-year-old females is recommended The choice between these two options should be based on genetic variability. Keywords." Dama dama mesopotamica, demographic stochasticity, extinction, Persian fallow deer, reintroduction. INTRODUCTION Reintroducing animals to areas within their former range is an attractive approach to saving endangered species. However, many reintroductions fail (Kleiman, 1989), and in most cases the reasons for failure are unknown. The Persian fallow deer Dama dama mesopotamica, once abundant throughout western Asia, is now one of the rarest deer in the world. Population numbers have declined throughout its range due to human expansion and hunting pressure. The last sightings of fallow deer in the wild in the region of Israel were made in the 19th century: yon Schubert reported sighting a fallow deer in 1837 in the Mount Tabor region of Palestine (Paz, 1980), and Tristram (1884) reported sightings in the same region in 1866. Several small populations were reported in various locations in Iran and Iraq in the early part of the 20th century, but by 1940 the Persian fallow deer was 27

28

D. Saltz 100

9O

females

males ~.~ 80- total

o . •

/ /

f /

0

~ 4o ~

30

~

20

0

.

,

,

1

,

1980 1982 1984 1986 1988 1990 1992 1994

YEAR Fig. 1. Number of adult Persian fallow deer at Hai-Bar Carmel breeding core, Israel. is to changes in the age structure. The size of the herd required to achieve a predetermined EP over a specified time period can then be estimated for each age structure. Based on these results a herd can be selected in a manner that will minimize the impact on the age structure of the source population. Here I report the results of such simulations used for selecting the females for a herd of Persian fallow deer to be reintroduced in Israel.

METHODS The data

There are no data on the dynamics of Persian fallow deer in the wild. At the Hai-Bar Carmel core the fallow deer are kept in large groups, and until recently were not marked. Therefore there is little information on age-dependent RS and survival. However, information is available from the world zoo herd as documented in the world studbook (Rudloff, 1991-93). I used these data to estimate survival curves, using animals with known birth and death dates or documented as still being alive in 1992. Age-dependent RS and progeny sex ratio were determined using those cases where the mother's birth date was known. I then constructed a life table for females. The modal

This life table was used in a Monte Carlo Leslie matrix simulation model to predict the future growth and EP arising from random demographic processes of various hypothetical reintroduced female populations of different size and age structure. I considered only females because fallow deer are polygynous, and unless all males disappear the number of males would have a minimal effect on the demography of the reintroduced population. Furthermore, as with other polygynous species, the breeding core of fallow deer at Hai-Bar Carmel has an excess of males, and adding males to the reintroduced population should not be a problem. The Leslie matrix does not consider density-dependent responses (and, therefore, requires no estimates of carrying capacity) and projects an exponential growth. Consequently, the technique is adequate only for short-

range projections of populations at the lower end of their growth curve. In this study I had no estimate of carrying capacity, the reintroduced population sizes were small, and density effects, therefore, presumed to be minimal. Previous reintroductions have documented a decline in reproductive success immediately following release into the wild, with gradual recovery over a period of several years (Saltz & Rubenstein, 1995). I incorporated such a response into my model by multiplying reproductive success by 0.2, 0.4, 0.6 and 0.8 for the years 1 4 following release, respectively. Population growth was projected over a period of 100 years. I selected this relatively short time frame because demographic stochasticity has a significant impact only when populations are very small (May, 1991). Thus, most extinctions caused by demographic stochasticity in reintroduced populations are expected immediately, or shortly, after reintroduction. The size of the population was recalculated yearly. Stochasticity was incorporated by having the survival of females and production of a female offspring varying as random binomials around the mean values found in the studbook population. Specifically, the program generated two random numbers from a uniform distribution between 0 and 1 (one for survival and one for reproduction) for each individual each year (Simberloff, 1988). If the first generated value was less than the survival rate for that specific age group, the female in the model survived to the following year. Similarly, if the second random number was smaller than the probability of an adult female in that age group producing a female offspring, such an offspring was added to the model's population. Environmental stochasticity and genetic effects were not incorporated into the model because insufficient data were available for describing these effects. Simulations

I estimated the best female group structure by simulating the release of 12 females using different age structure combinations. Generally, prime-aged females, i.e. young females after first parturition, are expected to produce the lowest EP. Fallow deer give birth for the first time at age 2. Therefore, assuming that the sex ratio of progeny was not age-dependent, the lowest theoretical EP would be achieved by releasing 12 2-yearold females after they have weaned their first young. If 2-year-old animals are limited, however, older age groups will have to be substituted and the structure will become closer to the age structure found in the parent population. In certain species the sex ratio of progeny may depend on maternal age (Saltz & Rubenstein, 1995). This is expected in species where the variance in male RS is considerably greater than that in females (Trivers & Willard, 1973), as is the case with European fallow deer D. d. dama (Apollonio et al., 1990). If prime-aged females tend to produce male offspring, lower extinction rates may be achieved by releasing subadults that produce mostly female offspring when they are primiparous. In

Minimizing extinction in reintroduced Persian fallow deer

29

Table 1. Extinction la'obability due to demogralsi~c stuehasticity as determined for nine different female age structures in a reintroduced population Monte-Carlo Leslie matrix simulations were used, with 1000 runs for each age structure. Numbers in the age columns represent the number of females in each age group used in each simulation, EP is extinction probability over 100 years for the specified age structure with 12 released animals. N(EP{0.0I ) is the number of animals needed for the specified age structure to achieve a 0-01 extinction probability over 100 years. The last two age structures represent old mother-subadult daughter pairs. In the pair with the asterisk, reproductive success of the daughters is not affected by the release process (see text for further details). Age 0

1

2

3

12 7 6 5 4 3 3

5 4 4 3 2

4

2 2 2 2 3

5

1 2 2

6

1 1 2

7

1

8

9

10

1 2

11

1

1

*6 6

such cases, the reintroduction of subadults would be advantageous only if their RS was not affected by the reintroduction process, e.g. they may have lower fidelity to their original home range and the transfer is less stressful for them. If, on the other hand, they need their mothers with them, this would increase the probability o f inbreeding depression and result in low genetic variability, unless older mothers, whose future RS would be negligible, are selected. Based on the above I used seven different age structures ranging from 12 2-year-old females through a range of ages in a roughly normal structure (Table 1). In addition, I used two more age structures consisting of six 12-year-old mother-subadult daughter pairs. In the first of these I assumed the RS of subadult daughters is not affected by the reintroduction, and in the second I assumed a decline in RS following reintroduction, as described above. One thousand replications were run for each age structure (Harris et al., 1987). I calculated EP as the percent of runs ending with < 1 animal. I then varied the size of the group while maintaining, as much as possible, the same age structure until EP over the next 100 years fell to just below 0.01. Mace and Lande (1991) recommend that a population be labelled as 'vulnerable' (the lowest levels of threat to a population) if it has a 0.1 EP within 100 years. I selected a more conservative value for two reasons: (1) the model considered only demographic stochasticity, and other sources of threats to the population, such as environmental stochasticity, were not included; (2) in view of the cost, effort, and rareness of animals involved, it is necessary to try and minimize EP as much as possible.

12

6 6

EP

N~EPI0.Ol )

0.016 0.014 0.018 0-016 0.030 0.048 0.066 0-034 0-080

14 13 13 15 16 17 26 16 > 30

females (82% vs. 66%, g 2 = 4.851, n : 169, p = 0.028). Excluding fawns, survival as a function of age was roughly linear and similar in both sexes up to age 9. Subsequently, mortality increased dramatically in males and decreased in females until age 15 when it plummeted; but sample size for these age groups was small and, therefore, confidence intervals large. There are no recordings of animals surviving past age 16. Except in very rare cases fallow deer produce no more than one fawn a year (Zuckerman, 1953), but may produce in consecutive years. RS changes with age (Fig. 3) and could be divided into three age groups with different RS 0( 2 = 6-101, d.f. : 2, p : 0.047): (1) does aged 6-10 with highest mean RS (0-82, n = 66); (2) does aged 2-5 (RS = 0.68, n = 96); and (3) does aged 11+ (RS : 0.59, n = 27). Overall progeny sex ratio was 1-21 (74~ :61 9) and did not differ significantly from 1:1 (X2 = 1.25, p -0.263, for mothers of known age). Progeny sex ratio was not related to maternal age (X2 = 5.66, d.f. = 7, p : 0.580). However, a pattern was evident (Fig. 4), suggesting that the lack of significance may be due to low statistical power. Because I was concerned with committing a Type II error (P~, the probability of failing 90

~'

• ~ males - . females simulated

~'

50

* "~

~30 20 10

RESULTS Dynamics Survival of fawns up to age 1, as determined from the studbook, is 75% (Fig. 2), with males faring better than

0

0

2

4

6

8

10

12

14

16

AGE Fig. 2. Survival curves of males and females according to studbook (solid line), and the survival curve for females used in the model described in the text (dotted line).

30

D. Saltz

the ages 1 and 9 that was fitted to the survival of the studbook females. An exponential decrease in survival was assumed from age 9+, from 91% to 87, 79, 63, 31, and 0% at age 14 (Fig. 2), i.e. I assumed maximum survival of females in the wild to be 2 years shorter than that documented in the studbook.

0.9 "0.S 0.7 0.6 0.5 0.4

Simulations

~ 0.3 ~

0.2

~

0.1 0

1 2 3 4 5 6 7 8 9 10 11 12 13 1415+

MOTHER'S AGE Fig. 3. Age-dependent reproductive success of Persian fallow

deer females according to the world studbook. Numbers over bars are sample size, i.e. number of females.

to reject the null hypothesis when it is false), I estimated the power (1-P~) of my test with Monte Carlo simulations (White, 1992). In these simulations I generated 300 random binomial data sets of similar sample size and structure, using the progeny sex ratios and sample size found in each of the eight age groups of mothers (Fig. 4) to generate the random numbers. In 93 of the 300 simulations progeny sex ratio was not significantly related to maternal age (P~ = 0.31), suggesting that if such a pattern existed I would have only a 70% chance of showing it. Based on this low power, I decided to include progeny sex ratios as a function of maternal age in my estimations of EP. Life table The mean RS for the three age groups described above (2-5, 6-10, and l l+) was multiplied by the progeny sex ratio for each age group to determine the production of female offspring. The plateau in the survival curve of mid-aged fallow deer is typical of many ungulate species (Pianka, 1978); however, its extenuation into older age groups is not typical of wild ungulates in which a sharp decline usually begins around 50-70% of the maximum expected life span. I constructed a survival curve using the actual survival of fawns, followed by an asymptotic curve of 93% survival/year between

O ;g

O a~ 2

3

4

5

6

7

8-11

12+

MOTHER'S AGE Fig. 4. Progeny sex ratio of Persian fallow deer as a function of mother's age based on the world studbook. Numbers in bars are sample size. ~], males; 1~, females.

Due to the assumed reduction in reproductive success following reintroduction, all simulated populations exhibited an initial decline. This decline was of shortest duration in the population started with 12 2-year-old females. Although an age-dependent sex ratio was assumed for the progeny, age structures consisting of male-producing age groups had the lowest EP (Table 1). There was little difference in EP between a herd of 12 females consisting of only 2-year-old animals and a combination of 2-5 year-old females. Once older age groups were included, EP began to increase. The number of females required to achieve an EP of 0.01 or less over 100 years increased gradually as older age groups were incorporated, usually requiring one additional female for each age group added. The use of six subadult females with their 12-year-old mothers, and assuming the RS of the daughters was not affected by the reintroduction process, produced an EP of 3.4%. This would require the release of 16 females (eight pairs) to achieve 0-01 EP over 100 years. If the reintroduction process does affect the RS of the daughters, EP for six pairs would increase to 8%, and more than 15 pairs would be needed for a 0.01 EP. DISCUSSION Demographic, genetic, and environmental stochasticity all play a role in the survival of small populations (Shaffer, 1981). Of these, demographic stochasticity is paramount when the population is smaller than 50 individuals (Nunney & Campbell, 1993). Reintroduced vertebrate populations often number less than 50. Consequently, demographic processes are expected to be a key factor in determining the success of the reintroduction, and should be a major consideration when selecting animals for release. While it is not possible tO prevent stochastic demographic events, one may reduce their impact by (a) releasing a larger population, and (b) increasing their RS and survival by selecting the correct age structure and appropriate animals (in terms of health and social structure). Since the number of animals released is often limited by availability, the age structure, specifically that of the females, is vital. While a normal age distribution is intuitively the best choice when social structure is considered, most ungulate reintroductions have selected prime-aged females for release (LeaderWilliams, 1988; Stanley Price, 1989). Older animals have a shorter life expectancy and lower RS. Subadults have no previous record of RS, may exhibit delayed RS in the absence of adults (Stanley Price, 1989), and may tend to disperse (Jameson et al., 1982). The selection of

Minimizing extinction in reintroduced Persian fallow deer prime-aged females, however, may result in progeny with a male-biased sex ratio (Saltz & Rubenstein, 1995), which will reduce population growth and increase probability of failure. Furthermore, selecting all prime-aged females may not be feasible due to limited availability. Based on my simulations, a 0.01 EP over 100 years can be achieved with a minimum of 13-14 adult females aged 2-4. If the number of available animals in these age groups is limited, older animals will have to be substituted and the size of the reintroduced herd increased to achieve an EP of 0.01. However, only a few animals will have to be added as long as age structure remains skewed towards the younger age groups, and all females are 8-years-old or younger. Because there are no data on age-related RS from Hai-Bar Carmel, it is difficult to make comparisons with the RS in the studbook. Overall RS based on studbook data was lower than that in Hai-Bar Carmel (0.71 vs. 0.78 fawns/doe/year, respectively). Thus, my estimations of herd size required for an EP of 0.01 may be somewhat larger than needed, though this is better than one that is too small. Reproductive success at the Hai-Bar Carmel increased from 0.55 fawns/doe/year in 1980-89 to 0.80 in the years 1990-94 (Fig. 5). Combined with the increase in the size of the herd this has produced 8-11 females each year. In most years prior to 1990, less than three females/year were born. If a reintroduction is targeted for 1995 it is not recommended that age groups older than 5 be included. Selecting only 2-year-old females is not feasible because 14 would be required to achieve an EP of 0.01. Thus, two options remain, releasing 2- and 3-year-old females or 2-,3- and 4-year-old females. In the first case, eight aged 2 and five aged 3 will be required to achieve an EP of 0.01, and in the second case seven aged 2, four aged 3, and two aged 4. The choice between the two will probably be based on the genetic variability that can be achieved in each case (see below). In species where variance in male RS is greater than that of females, mothers in better than average condition are expected to produce male offspring (Trivers & Willard, 1973). In several species of ungulates maternal r.~

1.2

(~

1.1

4

4

/

16 ~

0.9 0.8 0.7

10

© o.3 ~

0.2

~

0.1 0 1981

i 1982

1984

i i i J i , , i , 1986 1988 1990 1992 1994

YEAR Fig. 5. Annual reproductive success of Persian fallow deer females at Hai-Bar Carmel. Numbers over each point are sample size, i.e. number of females 2-years old or older.

31

age is associated with progeny sex ratio. These include Grevy's zebra Equus grevyi (Hayward, 1987), Peary and barren-ground caribou Rangifer taradus pearyi and R. t. groenlandicus (Thomas et al., 1989), and domestic sheep Ovis aries (Kent, 1992). Although I have not been able to show such a relationship in Persian fallow deer, the pattern suggests that such a relationship may exist, and the lack of significance is due to low statistical power. If subadult females that are released with their mothers do not exhibit a decrease in RS following reintroduction such a herd structure should be considered. Although 16 animals would be required to achieve the EP specified, eight of these would be older females that would have already contributed to the breeding core and whose future reproductive contribution would be limited. Thus, I recommend that several such pairs be included in later releases to test this hypothesis. In addition to demographic stochasticity, two other stochastic factors must be considered in the selection of a herd for reintroduction (Kleiman, 1989; Stanley Price, 1989): genetic and environmental. Small populations are expected to lose genetic diversity rapidly and have a high probability of deleterious genes being expressed due to inbreeding (Rails et al., 1979; Mace, 1986). To minimize these effects a herd that is as genetically diverse as possible must be selected for reintroduction. Because the breeding of fallow deer at Hai-Bar Carmel has not been controlled the herd's genealogy is unknown. Consequently we are using DNA fingerprinting techniques (Wayne et al., 1994) to determine the relatedness and genetic structure of the herd. Preliminary results from eight animals indicate that the genetic variability of the Hai-Bar herd is extremely low (average band sharing was 91% with 158 bands; Hillel, 1992). This is expected as a result of the bottlenecks that the Hai-Bar herd has gone through: (a) the original herd in the wild consisted of approximately 25 animals; (b) the world captive herd was founded from two males and one female trapped from the wild herd; and (c) the Hai-Bar herd was founded from five females and two males from the world herd. On the other hand, the high level of inbreeding is expected to have removed most deleterious genes, a hypothesis that is supported by the high RS of the Hai-Bar herd. We have no estimate of the impact of environmental stochasticity on the RS and survival of Persian fallow deer. A reintroduction programme submitted to the Israel Nature Reserves Authority (Saltz et al., 1994) has offered six alternative locations in northern Israel for the reintroduction. The locations were graded based on vegetation, water availability, corridors to adjacent natural areas, and human interference. Of these areas, Nahal Kziv Reserve in the western Galilee was selected. Post-release monitoring will provide some of the data necessary to assess environmental impacts, and from these data the model can be modified and supplementary releases carried out if necessary. The low genetic variability may make the Hai-Bar population susceptible to environmental stochasticity, thus increasing

32

David Saltz

EP in the reintroduced herd. Importing other strains would have a significant contribution. However, all animals of the world herd are from the same ancestry, and the chances o f obtaining 'new blood' from Iran are low. Consequently, although the genetic situation reduces the feasibility of success, there is little hope for change and we must make do with what is available. Male mating success o f European fallow deer is highly skewed (Apollonio et aL, 1990; Thirgood, 1990), with dominant lek males having the highest success, followed by single territory holders, a n d subordinate lek males having the lowest mating success. Thus, effective population size of the released herd may be considerably smaller than the actual number of animals released, increasing the rate of loss of genetic variability. A high buck/doe ratio may induce fast turnover in male dominance and therefore increase effective population size. On the other hand, such a ratio may also destabilize the herd during the critical post-release period (Sinai, 1994). Because demographic factors appear to be far more important than genetic factors in determining the success of a reintroduction during its initial stages (Nunney & Campbell, 1993), the initial release will have a low buck/doe ratio (four bucks to be released with the 12 does). Once the herd is well established, more bucks can be released in an effort to increase buck turnover rate. The model used suggests that at least 13 females aged 2-4 will be required to achieve an EP of 0.01 over the next 100 years. The numbers of female Persian fallow deer in these, and younger age groups that are presently at the Hai-Bar Carmel, suggest that this breeding core is capable of supporting a reintroduction at this time. However, if genetic and environmental stochasticity have a considerable effect on RS and survival, the herd may have to be increased to maintain an E P of 0.01 over 100 years. Such effects can only be determined after reintroduction, and can be buffered by future supplementary releases.

ACKNOWLEDGEMENTS My thanks go to the staff at Hai-Bar Carmel: Avinoam Lourie and Yaakub Maklade. Dr Mary Rowen and two anonymous referees reviewed the manuscript and provided helpful suggestions. The Schussheim Foundation has made significant contributions to Hai-Bar Carmel and the fallow deer reintroduction project.

REFERENCES Apollonio, M., Festa-Bianchet, M., Mari, F. & Riva, M. (1990). Site-specific asymmetries in male copulatory success in a fallow deer lek. Anim. Behav., 39, 205-12. Chapman, D. & Chapman, N. (1980). The distribution of fallow deer: a worldwide review. Mammal Rev., 10, 62-138. Harris, R. B., Maguire, L. A. & Shaffer, M. L. (1987). Sample sizes for minimum viable population estimation. Conserv. Biol., 1, 72-6. Hayward, L. (1987). Worm studbook of Grevy's zebra (Equus grevyi). Marwell Zoological Park, Hampshire, UK.

Heidemann, G. (1994). Situation of Persian fallow deer (Cereus dama mesopotamica) in Iran 1994. Institut for Haustierkunde, Christian-Albrechts-Universitat, Kid (unpublished report). Hillel, Y. (1992). A preliminary analysis of the genetics of the Hai-Bar fallow deer herd. Nature Reserves Authority, Jerusalem (in Hebrew) (unpublished report). Jameson, R. J., Kenyon, K. W., Johnson, A. M. & Wight, H. M. (1982). History and status of translocated sea otter populations in North America. Wildl. Soc. Bull., 10, 100-7. Jantschke, F. (1991). Persian fallow deer (Dama dama mesopotamica) at the Opel-Zoo Kronberg - - a history and critical evaluation. In International studbook of Persian fallow deer, No. 1, ed. K. Rudloff. pp. 15-19. Tierpark Berlin, Berlin. Kent, J. P. (1992). Birth sex ratios in sheep over six lambing seasons. Behav. Ecol. Sociobiol., 30, 151-5. Kleiman, D. G. (1989). Reintroduction of captive mammals for conservation. BioScience, 39, 152-61. Leader-Williams, N. (1988). Reindeer in South Georgia. Cambridge University Press, Cambridge. Mace, G. M. (1986). Genetic management of small popula* tions. Int. Zoo. Ybk, 24/25, 167-74. Mace, G. M. & Lande, R. (1991). Assessing extinction threats: toward a reevaluation of IUCN threatened species categories. Conserv. Biol., 5, 148-57. May, R. M. (1991). The role of ecological theory in planning re-introduction of endangered species. In Beyond captive breeding: re-introducing endangered mammals to the world, ed. J. W. H. Gipps. Clarendon Press, Oxford, pp. 145-63. Nunney, L. & Campbell, K. A. (1993). Assessing minimum viable population size: demography meets population genetics. Trends Ecol. Evolut., 8, 234-8. Paz, U. (1980). The wildlife in the Land of Israel during the late Ottoman period. Land and Nature, 146-50 (in Hebrew). Pepper, H. J. (1974). The Persian fallow deer. Oryx, 7, 2914. Pianka, E. R. (1978). Evolutionary ecology. Harper and Row, New York. Rails, K., Brugger, K. & Ballou, J. (1979). Inbreeding and juvenile mortality in small populations of ungulates. Science, N. Y., 206, 1101-3. Reed, C. A. (1965). Imperial Sassanian hunting of pig and fallow deer, and problems of survival of these animals today in Iran. Postilla, 92, 1-23. Rudloff, C. (1991-1993). International studbook of the Persian fallow deer. Tierpark Berlin, Berlin. Saltz, D., Lourie, A. & Kaplan, D. (1994). The Persian fallow deer in Israel: a reintroduction program. Israel Nature Reserves Authority, Jerusalem (unpublished report). Saltz, D. & Rubenstein, D. I. (1995). Population dynamics of a reintroduced Asiatic wild-ass (Equus hemionus) herd. Ecol. Appl., 5, 327-35. Shaffer, M. L. (1981). Minimum population sizes for species conservation. BioScience, 31, 1314. Simberloff, D. (1988). The contribution of population and community biology to conservation science. Ann. Rev. Ecol. Syst., 19, 473-511. Sinai, J. (1994). A program for assembling a herd from a large herbivore breeding core, for the purpose of reintroduction - - the Asiatic wild-ass Equus hemionus in Hai-Bar Yotvata. MSc thesis, Hebrew University of Jerusalem. Stanley Price, M. R. (1989). Animal re-introduction: the Arabian oryx in Oman. Cambridge University Press, Cambridge. Thirgood, S. J. (1990). Alternative mating strategies and the reproductive success in fallow deer. Behavior, 116, 2-9. Thomas, D. C., Barry, S. J. & Kiliaan, H. P. (1989). Fetal sex ratios in caribou: maternal age and condition effects. J. Wildl. Manage., 53, 885-90. Tristram, H. B. (1884). The fauna and flora of Palestine. London. Trivers, R. L. & WiUard, D. E. (1973). Natural selection of parental ability to vary sex ratio of offspring. Science, N. Y., 179, 90-2.

Minimizing extinction in reintroduced Persian fallow deer Wayne, R. K., Bruford, M. W., Girman, D., Rebholz, W. E. R., Sunnucks, P. & Taylor, A. C. (1994). Molecular genetics of endangered species, In Creative conservation: interactive management of wild and captive management, ed. P. J. S. Olney, G. M. Mace & A. T. C. Feistner. Chapman Hall, New York, pp. 92-117.

33

White, G. (1992). Do pellet counts index white-tailed deer numbers and population changes?: a comment. J. Wildl. Manage., 56, 611-12. Zuckerman, S. (1953). The breeding seasons of mammals in captivity. Proc. Zool. Soc. Lond., 122, 827-950.