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Influence of environmental factors on a population of goitred gazelles (Gazella subgutturosa subgutturosaGüldenstaedt, 1780) in semi-wild conditions in an arid environment: a preliminary study
Journal of Arid Environments (1998) 39: 577]591 Article No. ae980420
Influence of environmental factors on a population of goitred gazelles ( Gazella subgutturosa subgutturosa Guldenstaedt, 1780) ¨ in semi-wild conditions in an arid environment: a preliminary study
O. B. Pereladova*, K. Bahloul†, A. J. Sempere†§¶, N. V. ´´ Soldatova‡, U. M. Schadilov* & V. E. Prisiadznuk* * All-Russia Research Institute of Nature Conservation, Sadki-Znamenskoye, Vilar, Moscow, 113628, Russia † CEBC, CNRS, F-79360, Villiers en Bois, France ‡ Ecocentre ‘‘Goitred gazelle’’, Bukhara, Kagan, 705014, Uzbekistan (Received 9 November 1996, accepted 18 April 1998) A population of goitred gazelles ( Gazella subgutturosa subgutturosa Guldenstaedt, 1780) has been created and maintained in the Bukhara Breeding ¨ Centre, Uzbekistan since 1977. Population dynamics and range usage have been analysed for the period from 1978 to 1995. In 1989 the population in 5126 ha of the reserve peaked at 1224; in 1995 it was 580. Breeding success was correlated with meteorological conditions and was density-dependent. Changes of plant associations, connected with the gazelles population growth, are discussed. q 1998 Academic Press Keywords: goitred gazelle; population dynamics; breeding success; arid environment; rainfall; Uzbekistan
Introduction Because of competition with cattle and sheep, and also because of overhunting and poaching, different subspecies of goitred gazelle Gazella subgutturosa Guldenstaedt, ¨ 1780 (Geptner et al., 1961) are endangered everywhere in Asia (Wang et al., 1997). One of the subspecies, G. s. marica, is included in the Red Data Book of IUCN (IUCN, 1978, 1992) and another one, G. s. subgutturosa, in the Red Data Book of the USSR (USSR, 1984) and Red Data Books of all the states of the Central Asian part of U.S.S.R., in the limits of its area. In fact the situation in Central Asia is even worse. § Address for correspondence: Dr Antoine Sempere, ´ ´ Villiers en Bois, F-79360, France. ¶ Present address: Bureau CNRS in Moscow, app. 109, 14, ul. Goubkina, 117312, Moscow, Russia. 0140]1963r98r040577q15 $30.00r0
q 1998 Academic Press
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Gazelles inhabit 0.3% of the area they previously occupied in Caucasus and Tadjikistan, and their ranges have been halved in Kazhakstan and reduced even more in Uzbekistan and Turkmenistan (Flint & Prisiadzniuk, 1986). Wildlife in such areas can only be reintroduced if the probable causes of the decline of gazelles are eliminated, and if the group of animals released is numerically strong. To re-establish the goitred gazelle in its native area, special breeding centres were created with the main objective of developing the gazelle population in controlled areas. The first and largest of the centres created in the Middle Asian part of the former Soviet Union was the Bukhara Breeding Centre, Uzbekistan. This centre presents a wide range of conditions, the north being completely arid, and the south having higher biodiversity and some lakes which are connected with the underground water, itself fed by the Amou]Bukhara Canal. Such a range is highly desirable in arid environments where vegetation production is highly dependant on irregular rainfall (Nagy, 1988). This investigation considers the dynamics and adaptation to an arid environment of the present population, which is descended from the founder group of hand-reared animals. Correlation of population growth with seasonal rainfall, in relation to the reproductive cycle (breeding season, gestation, lactation) was investigated to establish the extent to which reproductive success of this population depended on population density andror environmental factors (rain, temperature, food).
Materials and methods This study was conducted in the southern Kyzylkum Desert at the Bukhara Breeding Centre, Uzbekistan (408 N, 658 E) which was established in 1978 with the main purpose of breeding goitred gazelles in intensive husbandry for repopulating their optimum habitat, the desert. The centre comprises fenced territory of 5126 ha, pens and buildings, three observation towers and a system of lakes, connected by a canal and the underground water. The water is saline to the extent of 2 to 17 g ly1 (Prisiadzniuk, 1986) in its southern part. The length of the reserve is about 15 km from the north to the lakes in the south, and it is not wider than 3 km in the middle part.
Climate Meteorological data were obtained from Bukhara airport, 15 km from our reserve. During the 12 years from 1982 to 1994 most precipitation fell between December and May. Annual precipitation ranged from 78 mm (1989) to 245 mm (1993) with a mean ("SEM) of 158 " 10 mm. The dry period lasts from April to November (-20 mm monthy1 ) (Fig. 1). Maximum temperature occurs in July (mean 298C) when the highest daily temperature reaches 408C to 468C (42.5 " 0.48C). It is coldest during December and January, when minimum daily temperature falls to y88C to y258C. Snow is very rare (once in 4]6 years) and fallen snow does not persist.
Vegetation The main zones of vegetation in the breeding centre are: hilly and undulating sandy plain; saline land; and saline lake depression. The plateau (rocky hill) is surrounded by the lower slopes of the main hill. The north of the reserve is mainly sand and gravel plain, whereas lakes are present in the south. There are ten main plant associations (Fig. 2; from Shenbrot, 1987; Mordonov,
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Figure 1. Climatic characteristics 15 km from Bukhara Breeding Centre in 1982]1994. (a) The three lines represent maximum (l), mean (') and minimum ()) monthly temperatures; (b) mean monthly rainfall " SEM. Asterisks indicate significant differences between consecutive months.
1993): riparian forests, with reeds, Phragmites communis, and tamarisk, Tamarix sp.; halophytic communities of the wetter saline lands}Halocnemum strobilaceum, Kalidium spp., Hallostachys caspica, Suaeda spp., Gamantus owimus; plant associations of compressed gypsum sandy loam and loamy soil plains}Zigophyllum spp., Alhagi pseudalhagi, Aelenia spp.; plants of sandy loam and loamy hills}Salsola spp., Reamuria turkestanica; plant associations on the slopes of rocky hills on sandy-gravel loams}Artemisia terrae-albae, A. herba-albae, A. diffusa, Ephedra sp.; gypsophilic plant associations on the rocky tops of hills}Salsola spp., Convolvulus spp., Astragalus spp.; sandy-gravel soil associations on the cones of valleys}Stipa gogenacerii, Calligonum junceum; psammophilic vegetation of the bottoms of valleys}Aristida pennata, Smirnovia turkestana; plants of undulating sandy plains}Ammotamnus
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Figure 2. Plant associations in the Bukhara Breeding Centre: 1 s lakes; 2 s riparian forests (reeds, tamarisk); 3 s halic plants of clay or wet saline lands; 4 s plant associations of compressed gypsum sandy loam and loamy soil plains; 5 s plants of sandy loam and loamy soil hills; 6 s plant associations on the slopes of rocky hills on gravely-sandy loams; 7 s gypsophilic plant associations on the rocky tops of hills; 8 s sandy-gravely soil associations in the cones of valleys; 9 s psammophilic vegetation of the valley bottoms; 10 s plants of undulating sandy plains; 11 s plants of hilly-sandy plains; 12 s plant-free areas. (For the plant associations themselves, see in the text.) 13 s observation towers. A]J, 0]30 s network for mapping animals.
lemanna; and plants of hilly-sandy plains}Salsola spp., Astragalus spp., Convolvulus hammsola, Artemisia diffusa. Cover abundance of the vegetation is 5]75%, and the productivity varies from 190 to 620 kg hay1 (dry weight) depending on the plant association with variation between years. Variation of productivity in one and the same association can vary 4]5 fold between years due to ephemeral vegetation, depending on the humidity and temperature in spring, and local productivity of up to 1279 kg hay1 on the mountain slopes and up to 2186 kg hay1 on the saline-land depression in favourable years has been recorded (Mordonov, 1993).
Animals Forty-four goitred gazelles ( Gazella subgutturosa subgutturosa, Guldenstaedt, 1780) (21 ¨ males and 23 females) aged 1]2 (20%), 3 (40%) and 4]5 (40%) years, were collected and hand reared in different areas of Uzbekistan and were set free on the main territory of the breeding centre in May 1977. Five of them had been injured during transportation, so it is unlikely that they survived very long. The animals were set free 2 km from the buildings of the centre and about 1 km from the main watering places
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(C3, Fig. 2). Within a few weeks of their release into the centre in 1977, the flight distance of the gazelles increased from some dozens of metres to approximately 500 m. Female goitred gazelles in native populations usually become fertile at the age of 18]19 months, but occasionally at 7]8 months, if their weight reaches 16 kg. Males only become fertile at 18]19 months. Breeding takes place from the end of November to mid December, or sometimes till the beginning of January (with some variations in different populations), gestation lasts from 148 to 163 days, and parturition occurs during late April and May. As many as 75% of females in a population may produce twins, although single fawns are typical for the first parturition and for the majority of females in less favourable conditions. The main period of lactation lasts 65 to 80 days, although some fawns continue to suck until October (Geptner et al., 1961; Djevnerov, 1984; Kutcheruk, 1995). In order to determine the size of the population in the centre, censuses have been made yearly in October since 1981 (Flint et al., 1986). (There was no exact census on the growth of the group in 1979]1981; data were obtained just by observations from towers.) The census proceeded as follows: (1) route census in the north part of the centre, observers (7]8 persons) keeping in visual contact with each other while moving along parallel routes from the north border to a line of hides in the middle of the centre; (2) driving animals from the southern part of the centre, about 20 persons moving from the southern border to the north along parallel routes at a distance of 200}250 m from each other; (3) driving animals from the southern part of the centre along the open middle part through the line of hides, with animals passing between hiding places being counted and age and sex noted. During this census, dead animals were recorded. Only two age classes have been distinguished: adults (more than 15 months, potentially reproducers) and fawns (about 5-months-old). Sex is determined easily for adults (only males have horns) but is not possible for fawns during the census. An annual reproductive index was calculated, defined as the number of fawns divided by the number of adult females. This global index includes fecundity, neonatal survival and percentage of reproductive females. The area was divided into three zones: south (up to A7]J10), middle (up to A16]J17) and north. Population densities and animal distribution for each zone were deduced by observations from the three observation towers (Fig. 2) (Flint et al., 1986) and by the density of faeces (Mordonov, 1993). As the fence was not truly repaired for a long time, some occasional emigration of animals occurred beginning in 1984, being registered by density of tracks crossing the border (not exact number of animals, but approximate amount}single, dozens, hundreds).
Statistical analysis All data have been analysed using Simstat 1997. After verification of no correlation between climatic variables, we used step by step multivariate regression analysis to explore the relationships between reproductive index and the following variables (only three of them are explanatory): population density (one variable), bimonthly mean temperature (six variables) and bimonthly number of rainy days (six variables). Growth rate of the population has been assessed by a linear regression of the population size from 1977 to 1989, the period leading to the highest population. Negative residuals appear in 1987, so we have divided the two periods for further comparisons (before and after 1987) assuming a change in population dynamics.
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Table 1. Growth of gazelle population in the Bukhara Breeding Centre from 1977 to 1995
Year
Population
1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995
44 49 71 108 186 271 410 606 580 721 900 1137 1224 1008 814 916 628 712 580
Growth rate
Index of reproduction*
0.114 0.449 0.521 0.722 0.457 0.513 0.478 y0.043 0.243 0.248 0.263 0.077 y0.176 y0.192 0.125 y0.314 0.134 y0.185
0.705 0.86 0.879 0.87 0.97 0.36 0.446 0.607 0.703 0.417 0.27 0.569 0.286 0.508
* Number of fawns divided by number of adult females.
Mann-Whitney tests were used to compare the reproductive indices of the population and fawn proportions within the two periods. Chi-square ( x 2 ) tests were used to compare the density of the populations in the three zones of the reserve during the two periods. Results Population growth From 1977 to 1989, a period of 12 years, the population in the reserve grew from 44 to 1224, and then declined (Table 1, Fig. 3(a)). Until 1989, there was an exponential growth (ln( N ) s 0.3001 x y 19.23, r 2 s 0.9599) with a very high mean coefficient of population growth (1.32 " 0.22; Fig. 3(b)). After 1989 the population tended to ) ) decrease (mean coefficient s y0 .10 " 0 .19 from 1990 up to 1995) (Fig. 3(a-(c)), although variations between years were considerable. However, as early as 1987, growth rate slowed down, regression residuals of ln( N ) s f (year) becoming negative (Fig. 2). This allowed us to divide the period in two: before and after 1987. The reproductive index was high from 1977 to 1986 (Fig. 4). Breeding success was significantly higher between 1982 and 1986, 0.86 " 0.1, than between 1987 and 1994 when it decreased to 0.46 " 0.15 (U s 0, p - 0.01). It corresponds to a mean of 29.8 " 2.6% of fawns in the total population in October before 1987, and 20.3 " 8.1% after 1987. During the whole period of the study (1977]1995), the percentage of animals found dead in the reserve was almost always less than 10%. The causes of mortality are not known. Of the dead animals, 42% were fawns and 58% were adults and sub-adults.
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Figure 3. Development of the gazelle population in Bukhara Breeding Centre from 1977 to 1995 (data of October census). (a) Changes in the number of animals registered during the census; (b) index of population growth in 1977]1989; (c) growth rate of the population ( NxrNxy1 , where N s number of animals registered during the census; x s a year of census, and x y 1 s previous year).
In consequence of the decrease of breeding success beginning in 1986, the percentage of fawns decreased from a mean of 31.2% before 1987 to 17.5% after 1987. The sex ratio of adults remained around 1:1 often with slightly more females (53.9% " 1.1%) from 1987 to 1995 (Fig. 5). This is similar to the sex ratio of the foundation group of animals introduced to the centre (52.3%; 21 male and 23 females). The distribution of the population between the three geographical zones of the centre remained practically stable between 1983 and 1989, keeping the same ratio from
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Figure 4. Index of reproduction (fawns per female in October).
the north to the south (1r4r10) ( x 2 test), although the total number of animals increased by three times (from 410 up to 1224). The decrease of population density from the south to the north is closely connected with the heterogeneity of the centre. The mean population density (animals per 100 ha) changed from 40 in 1983 to 123 in 1989 in the southern zone; from 18 to 54 in the central zone; and from 4 to 13 in the northern zone.
Environmental factors Multivariate regression step by step consists of three different explanations of the changes in reproductive index (IR): IR s y3 .5806 q ( 0 .1948 " 0 .06138 = TEMP89 ) q
( y0 .1265 " 0 .0422 = DRF67 ) q ( y0 .0003964 " 0 .000185 = POP ) R 2 s 0 .7150; to enter p s 0 .1; to remove p s 0 .15
Figure 5. Sex ratio of adult animals in the population in October (date of census): ( number of males; (- - - - -) s number of females.
)s
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Table 2. Analysis of the changes in reproductive index
Explanatory variables
Variable
Beta ( b )
Standard error SEM
Origin TEMP89 DRF67 POP
y3.5806 0.1948 y0.1265 y0.000396
0.0614 0.0423 0.00019
Correlation
Partial correlation coefficient
t
p
0.584 y0.3951 y0.4099
0.7268 y0.7064 y0.5809
3.174 2.994 2.141
0.0113 0.0151 0.0609
F
p
7.525
0.008
df.
F
Analysis of variances Source Regression Residual
df. 3 9
Sum of squares Mean square 0.4986 0.1988
0.1662 0.0221
Durbin]Watson test s 1.91 Summary of tests of changes Step 1 2 3
Variable
R2
qTEMP89 qDRF67 qPOP
0.341 0.5698 0.715
Change of R 2 0.341 0.2288 0.1452
1, 11 1, 10 1, 9
p
0 1 5.317 0.0438 4.584 0.0609
TEMP89 s mean temperature in August and September; DRF67 s days with rainfall in June and July; POP s size of the population in October.
where TEMP89 s mean temperature in August and September ( t s 3.521, p - 0.01; F s 12.399, p - 0.01), DRF67 s days with rainfall in June and July ( t s 3.254, p s 0.0116; F s 5.317, p s 0.0438), and POP s size of the population in October ( t s 2.858, p s 0.0212; F s 4.584, p s 0.0609). Variations of the equation are given in Table 2 ( b is a coefficient of a partial regression, which appears in the equation of regression). The step by step multivariate regression analysis proves a strong positive correlation of IR with temperature in August]September, and negative correlation with the number of days with precipitation in June and July and with the size of population. Table 3 presents excluded variables, which do not prove significant correlations with the reproductive index.
Discussion The new gazelle population introduced into the fenced area showed exponential growth from 1977 to 1987, which indicates that the population increased without any restraint. This makes it possible to examine specifically the potential for free growth in this goitred gazelle population, which is even higher (1.44}mean for the period 1977]1987) than in European roe deer (1.32; Gaillard, 1988) and Alpine ibex (1.28; Toıgo ¨ et al.,
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Table 3. Variables with no significant correlation with the reproductive index, rejected from the multivariate regression
Variables* temp 10]11 temp 12]01 drf 10]11 drf 12]01 drf 02]03 drf 04]05 drf 08]09 temp 02]03 temp 04]05 temp 06]07
F
p
0.375 0.188 2.719 1.769 0.019 0.02 1.471 0.001 0.361 0.093
0.5554 0.6748 0.1336 0.2162 0.8947 0.8896 0.256 0.9703 0.5626 0.767
* temp 10]11 s mean temperature of October]November, etc.; drf 02]03 s number of days with rainfall in February]March, etc.
1997) which are known to be the most efficiently reproducing wild ruminant species in Europe, and higher than the mountain gazelle of Saudi Arabia (1.32) which has two reproductive periods a year yielding a single fawn (Dunham, 1997). The phase of exponential growth from 1977 to 1983 coincided with occupation of the south zone of the Centre, and subsequently to occupation of the central and northern zones, which are ecologically less favourable for the animals (mainly due to absence of watering). The southern zone, being the most humid and thus the most rich in vegetation, supports the highest population density. Occupation of the whole area has been advancing step by step. The proportion of the population in each zone, reflecting ecological conditions, had remained stable through the years and at different absolute population densities. The population density in the south continued to grow until 1989 as the carrying capacity was not fully utilized. Emigration of animals since 1984 would correspond to the natural behaviour of spacial dispersion, and the high population density would amplify this phenomenon (Johst & Brandl, 1997). The level of population growth itself should be interpreted very carefully, taking into consideration different factors. It may be suggested that the population decrease after 1989 was connected with both emigration and with declining reproductive success (fertility of adults and survival of fawns). Mordonov (1993) interprets the seasonal disappearance of plant species preferred by gazelles from some places in 1989 (Prisiadzniuk & Soldatova, 1984) as a sign of overgrazing. Our results indicate an overstocking of the area (high number of animals, low reproductive index). Due to the decrease of breeding success and population growth since 1986, we suggest that the effect of population density was cumulated within the 3 years before 1989. This phenomenon may not have been limited to the southern zone. Although the population density, which was regularly checked by counting the amount of faeces (Mordonov, 1993), continued to grow, the proportion in each zone continued to be 1r4r10 in both 1983 and 1989 in favour of the south. If overpasturing took place only in the south, the proportion could change in favour of the north. This was not the case, so it is probable that the low amount of available vegetation in the north, combined with the long distances to watering places, could be a limiting factor for population density in the north. In any case, the stable proportion 1r4r10 indicates a parallel increase in pressure on available vegetation in all zones. Population density in the southern and central zones became higher than has been registered for mountain gazelles (15 gazelles 100 hay1 ) (Dunham, 1997), due to better
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food and water resources in these parts of the Centre. In the north it is different; here the local density does not reach those observed in Saudi Arabia, and is never higher than 12.8 gazelles 100 hay1 . It can thus be concluded that all the area of the reserve has been utilized since 1983 (equivalent proportion of local densities) and overexploited (negative residuals of regression, see above) since 1986. The recorded sex ratio of the population could be slightly biased in favour of females, as sub-adult males are often counted as females during the census. But still it remains around 1.17 females:1 male (see Fig. 5), which is similar to the proportion of the initially introduced group (1.1:1), and more equal than the reintroduced population of mountain gazelles in Saudi Arabia (1.6:1) (Dunham, 1997). The presence of a nearly equal number of males (who are utilizing the food resources) is not useful for the reproductive success of the population, and it increases the density-dependence of the population. In the population of mountain gazelles studied by Dunham, only 45% of males were territorial (that is reproductive), and so the corrected sex ratio for reproductive animals was 3.6:1, similar to the results obtained with other Antilopinae (4:1; Jarman, 1974; Wang et al., 1997). Similarly, we suggest that the high percentage of bachelor males andror non-territorial and opportunist reproductive males (Marmosinskaia, 1996) is very important for the dynamics of the population. Fluctuations of the number of animals around some optimum and sex ratio regulation can be achieved in populations in different ways. One of them, which is very important for open populations in nature, is emigration. In the Bukhara population this could play a part (Marmosinskaia, 1996; Soldatova & Bahloul, pers. obs.) because the enclosing fence had been damaged on occasion even before 1989, and was not regularly repaired. So emigration of young males since 1989 may have contributed substantially to the decline of the population. During the breeding season (November to December), male gazelles control their harem, moving around with it, when population density is low; when population density is high some males become territorial and participate in reproduction, while others remain mobile in non-reproductive bachelor groups (Mambetdjumaev, 1970; Gorelov, 1972; Djevnerov, 1984; Blank, 1985). In the Centre, territorial behaviour of males in November and December has been noted since 1985, at least in the southern part, and all over the Centre later (Marmosinskaia, 1990). This social interaction could therefore cause emigration (to the north and outside of the Centre), mainly of bachelors, from reproductive areas during the period of territorial behaviour. This kind of regulation of the male population could be beneficial for the breeding activity of the adult population, decreasing grazing pressure and the level of competition between males, and so reducing losses of energy of territorial males participating in reproduction and subsequent mortality level (Ralls et al., 1980; Promislow, 1992). The high percentage of fawns before 1987 (29%), which was similar to that recorded in the wild for Mongolian gazelles (Wang et al., 1997) and in introduced mountain gazelles (42%) (Dunham, 1997), seriously decreased after 1987 (20%). Interactions between females in the high-density population might have inhibited ovulation and consequently fertility (Alados & Escos, 1992). Moreover it may be that the presence of a high proportion of young adult females (connected with the rapid growth of the population during previous years), which are less productive than multiparous females, at least in related species (Olmedo et al., 1985; Alados & Escos, 1991; Langvatn et al., 1996), affected breeding success and therefore the percentage of fawns. At Bukhara two periods of vegetation growth are usually observed, in spring and autumn, with a quiescent period in summer. The best development of vegetation was observed in autumn, while 50% of living parts of plants was grazed in spring (Mordonov, 1993). Summer rain has a negative effect on the survival of fawns aged from 1- to 4-months-old, despite the increase of plant growth that occurs with high
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precipitation in an arid environment (Nagy, 1988). Some data indicate that thermoregulation in fawns is poor during the first month of life (Hull, 1973). According to our observations in 1996]1997 numerous animals were found dead in the Centre after heavy late spring and early summer rains. Moreover, according to previous investigations in pens at another breeding centre, there is a category of fawns that is exceptionally at-risk to die after rain (Pereladova, 1986). This could result from the effect of rainfall on heat loss, mainly during the night when there is a sharp fall in temperature, as has also been shown for sheep (Webb et al., 1984). In fact, rainy days in June and July can slightly reactivate the vegetation, which is usually absolutely dry in July and August, and consequently reduce the autumn forage production, which corresponds to the weaning period and the highest food requirements for the fawns. Moreover, summer rains encourage development of parasites, mainly in fawns (Masson, 1977), and can reduce or stop lactation further adversely affecting survival of fawns. Dry months (August and September) have a positive effect on breeding success (survival of fawns) and this is surprising after 3 months of dryness. High temperatures in early autumn stimulate vegetation growth (even without rains) and also delay the approach of winter. It should be especially emphasized that the intermediate seasons (autumn) are rather short in a continental climate and are challanging to animals. So, the occurence of a ‘prolonged’ summer allows fawns to achieve a body condition that is adequate (compensatory growth after weaning; Albon & Clutton-Brock, 1992; Andersen & Linnell, 1997) to allow survival during the early (November) and rather cold winters of the continental climate, by aiding thermoregulation of fawns at the beginning of the cold period. Population density (Table 2) has a low negative effect on breeding success. This was evident during the first period after introduction (1977]1983) when there was no density dependence (Johst & Brandl, 1997). Afterwards, an indirect effect of population density (limitation of food) could possibly affect the body condition of females and delay oestrus and so affect the survival of fawns in the next autumn (White, 1990). Lack of sensitivity of our index of reproduction could explain the relative independence of breeding success from density. Different components of the reproductive index (fecundity, neonatal mortality, post-weaning mortality) can compensate their individual variations, reducing the overall variation of the reproductive index induced by density ( Allaine ´ et al., 1992) . It seems that spring precipitation had no positive influence on breeding success, probably because of the low dependence of the vegetation in the southern part on rainfall, in contrast to that observed in the Arabian Desert (Dunham, 1997). Vegetation growth at Bukhara is more dependent on changes in the level of underground water and lakes inside the reserve which is artificially controlled by the level of the Amou]Bukhara Canal. Thus the amount of vegetation needed for normal lactation of gazelles in the first month is not dependant on rains in the most densely inhabited southern zone.
Conclusion Our investigations have shown that the breeding success of goitred gazelles in the Bukhara reserve is correlated with meteorological conditions (i.e. late spring rainfalls had a negative effect, while high autumn temperatures had a positive effect on body condition of fawns) and is density dependent. This preliminary study was made because this species, endogenous to Central Asia, must adapt to water restraint, as must African ungulates, and also to seasonally cold conditions of paleoarctic species. None of the existing theories on the growth of
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populations in an arid environment, which have been developed mainly on African models (living without cold seasons), could be utilized in our case. There have been studies on the ecology of populations of this type but because they have been published in Russian they are not widely known or used in the development of such theories. On the other hand, there are Russian works which develop theories of population dynamics, but deal with populations in forest and steppe zones, which are different in principal from arid conditions in continental deserts. So we could not use these theories either for interpreting our data on population development. Thus these original data can form the base for future development of a theoretical model. Another important conclusion is that the choice of reintroduction conditions (ecological conditions, size and sex ratio of the initial group, which define the growth of the group during the first phase of growth) may lead to a durable population structure, which does not necessarily correspond to a stable natural population (sex ratio, migration rate, breeding success). We are very grateful to the Ministry of Ecology of Uzbekistan, ‘Gosbiocontrole’, Mr A.K. Atadjanov and the Directors of the Bukhara Breeding Centre, for enabling our work to take place. We give special thanks to Natasha Marmosinskaia, Bakhtiour Mordonov and other staff of the Centre for collecting data and for participating in the census. We thank the specialists of the All-Russia Research Institute of Nature Conservation, led by Prof. V.E. Flint, for their help and participation in our work. We are also grateful to Dr J.M. Gaillard and Prof. H. Barre ´ for comments and corrections on statistical data, and the reviewers for their constructive comments. This analysis made possible by a grant from CNRSrMAE PICS 266. We thank Dr S.J.G. Hall for help in improving the manuscript.
References Alados, C.L. & Escos, J.M. (1991). Phenotypic and genetic characteristics affecting lifetime reproductive success in female Cuvier’s, dama and dorcas gazelles ( Gazella cuvieri, G. dama and G. dorcas ). Journal of Zoology, London, 223: 307]321. Alados, C.L. & Escos, J.M. (1992). The determinants of social status and the effect of female rank on reproductive success in dama and Cuvier’s gazelles. Ethology, Ecology and Evolution, 4: 151]164. Albon, S.D. & Clutton-Brock, T.H. (1992). Cohort variation in reproduction and survival: implications for population demography. In: Brown, R.D. (Ed.), The Biology of Deer, pp. 15]21. Berlin, Heidelberg, New York: Springer. 596 pp. Allaine, ´ D., Houssin, H. & Gaillard, J.M. (1992). Etude de la variabilite´ spatio-temporelle d’un indice de reproduction dans une population de chamois ( Rupicapra rupicapra). Gibier Faune Sauvage, 7: 85]94. Andersen, R. & Linnell, J.D.C. (1997). Variation in maternal investment in a small cervid; the effects of cohort, sex, litter size and time of birth in roe deer ( Capreolus capreolus ) fawns. Oecologia, 109: 74]79. Blank, D.A. (1985). Specificity of social and reproductive behaviour of gazelles ( Gazella subgutturosa) in the valley of Ili river. Zoologitcheskii Journal, 64: 1059]1070. (In Russian.) Djevnerov, V.V. (1984). Goitred Gazelle of Barsakelmes Island. Alma-Ata: Nauka. 144 pp. (In Russian.) Dunham, K.M. (1997). Population growth of mountain gazelles reintroduced in central Arabia. Biological Conservation, 81: 205]214. Flint, V.E. & Prisiadzniuk, V.E. (1986). Population condition, conservation and future of goitred gazelle restoration in the USSR. In: Flint, V.E. & Prisiadzniuk, V.E. (Eds), Conservation and Future Restoration of Goitred Gazelles in the USSR, pp. 3]8. Moscow: Gosagroprom. (In Russian.) Flint, V.E., Prisiadzniuk, V.E. & Soldatova, N.V. (1986). Bukhara breeding centre. Information
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4. Goitred gazelle census. In: Flint, V.E. & Prisiadzniuk, V.E. (Eds), Conservation and Future Restoration of Goitred Gazelles in the USSR, pp. 43]49. Moscow: Gosagroprom. (In Russian.) Gaillard, J.M. (1988). Contribution `a la dynamique des populations de grands mammiferes: ` l’exemple du chevreuil ( Capreolus capreolus ). Ph.D. thesis, University of Lyon, France. 308 pp. Geptner, V.G., Nasimovitch, A.A. & Bannikov, A.G. (1961). Mammals of the Soviet Union, Vol. 1, Ungulates. Moscow, High School. 714 pp. (In Russian.) Gorelov, J.K. (1972). Reproduction of goitred gazelles and the problem of its restoration in Badhis. Theriology, 1: 420]424. (In Russian.) Hull, D. (1973). Thermoregulation in young mammals. In: Whitton G.C. (Ed.), Comparative Physiology of Thermoregulation, pp. 167]200. IUCN (1978). Red Data Book of International Union for the Conservation of Nature, Vol. 1. Switzeland: Merdges. IUCN (1992). Red Data Book of International Union for the Conservation of Nature, Vol. 1. Switzeland: Merdges. Jarman, P.J. (1974). The social organisation of Antilope in relation to their ecology. Behaviour, 48: 215]267. Johst, K. & Brandl, R. (1997). Evolution of dispersal: the importance of the temporal order of reproduction and dispersal. Proceedings of Royal Society of London B, 264: 23]30. Kutcheruk, V.V. (1995). Goitred gazelles. In: Kutcheruk, V.V. (Ed.), Mammals of Turkmenistan, Vol. 1, Predators, Pinnipedia, Ungulates, pp. 222]237. Ashgabad: Ilym. (In Russian.) Langvatn, R., Albon, S.D., Burkey, T. & Clutton-Brock, T.H. (1996). Climate, plant phenology and variation in age of first reproduction in a temperate herbivore. Journal of Animal Ecology, 65: 653]670. Mambetdjumaev, A. (1970). Goitred Gazelles. Tashkent, Fan. 196 pp. (In Russian.) Marmosinskaia, N.V. (1990). Social behaviour of goitred gazelles during the reproductive period. V Congress of All-Union Theriological Society, Abstracts, 3: 32]33. (In Russian.) Marmosinskaia, N.V. (1996). Territorial and marking behaviour of goitred gazelles (Artiodactyla, Bovidae) in Bukhara breeding centre. Zoological Journal, 75: 142]156. (In Russian.) Masson, P.C. (1977). Gastrointestinal parasitism in red deer. New Zealand Journal of Agricultural Science, 11: 182]183 Mordonov, B.K. (1993). Goitred gazelle influence over the vegetation of deserts. Ph.D. thesis, Institute of Nature Conservation, Moscow. 26 pp. (In Russian.) Nagy, K.A. (1988). Seasonal patterns of water and energy balance in desert vertebrates. Journal of Arid Environments, 14: 201]210. Olmedo, G., Escos, J. & Gomendio, M. (1985). Reproduction de Gazella cuvieri en captivite. ´ Mammalia, 49: 501]507. Pereladova, O.B. (1986). Individual specificity of social behaviour of goitred gazelles. In: Flint, V.E & Prisiadzniuk, V.E (Eds), Conservation and the Future Restoration of Goitred Gazelle Number in the USSR, pp. 74]84. Moscow: Gosagroprom. 223 pp. (In Russian.) Prisiadzniuk, V.E. (1986). Bukhara Breeding Centre. Information 5. Watering places of goitred gazelles. In: Flint, V.E & Prisiadzniuk V.E (Eds), Conservation and the Future Restoration of Goitred Gazelle Number in the USSR, pp. 59]70. Moscow: Gosagroprom. 223 pp. (In Russian.) Prisiadzniuk, V.E. & Soldatova, N.V. (1984). Bukhara Breeding Centre. Information 1. Foraging of goitred gazelles in semi-wild conditions in sandy hills. In: Scientific Basis of Conservation and Sustainable Usage of Animals World, pp. 28]43. Moscow: VNII priroda. 275 pp. (In Russian.) Promislow, D.E.L. (1992). Cost of sexual selection in natural populations of mammals. Proceedings of the Royal Society of London B, 247: 203]210. Ralls, K., Brownwell, R.L. & Ballou, J. (1980). Differential mortality by sex and age in mammals. Report of the International Whaling Commission, Special issue, 2, pp. 223]243. Red Data Book of the USSR (1984). Moscow: Lesnaja promishlennost. 72 pp. (In Russian.) Shenbrot, G.I. (1987). The productivity of pastures and the role of rodents as food competitors of gazelles. In: Regional Aspects of Gazelle’s Biology. VINITI, 2745-B87, Moscow, pp. 105]113. (In Russian.) Toıgo, ¨ C., Gaillard, J.M. & Michallet, J. (1997). Adult survival pattern of the sexually dimorphic Alpine Ibex ( Capra ibex ibex ). Canadian Journal of Zoology, 75: 75]79
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Wang, X., Sheng, H., Bi, J. & Li, M. (1997). Recent history and status of the Mongolian gazelle in Inner Mongolia, China. Oryx, 31: 120]126. Webb, D.R., Dineen, J.K. & Kelley, J.D. (1984). Effects of wetting on insulation of bird and mammals coats. Journal of Thermal Biology, 9: 189]191. White, G.R. (1990). Nutrition in relation to season, lactation, and growth of north temperate deer. In: Brown R.D. (Ed.), The Biology of Deer, Proceedings of International Symposium on the Biology of Deer, Mississippi, 28 May]1 June 1990, pp. 407]417. New-York Inc: Springer-Verlag. 596 pp.
Influence of environmental factors on a population of goitred gazelles ( Gazella subgutturosa subgutturosa Guldenstaedt, 1780) ¨ in semi-wild conditions in an arid environment: a preliminary study
O. B. Pereladova*, K. Bahloul†, A. J. Sempere†§¶, N. V. ´´ Soldatova‡, U. M. Schadilov* & V. E. Prisiadznuk* * All-Russia Research Institute of Nature Conservation, Sadki-Znamenskoye, Vilar, Moscow, 113628, Russia † CEBC, CNRS, F-79360, Villiers en Bois, France ‡ Ecocentre ‘‘Goitred gazelle’’, Bukhara, Kagan, 705014, Uzbekistan (Received 9 November 1996, accepted 18 April 1998) A population of goitred gazelles ( Gazella subgutturosa subgutturosa Guldenstaedt, 1780) has been created and maintained in the Bukhara Breeding ¨ Centre, Uzbekistan since 1977. Population dynamics and range usage have been analysed for the period from 1978 to 1995. In 1989 the population in 5126 ha of the reserve peaked at 1224; in 1995 it was 580. Breeding success was correlated with meteorological conditions and was density-dependent. Changes of plant associations, connected with the gazelles population growth, are discussed. q 1998 Academic Press Keywords: goitred gazelle; population dynamics; breeding success; arid environment; rainfall; Uzbekistan
Introduction Because of competition with cattle and sheep, and also because of overhunting and poaching, different subspecies of goitred gazelle Gazella subgutturosa Guldenstaedt, ¨ 1780 (Geptner et al., 1961) are endangered everywhere in Asia (Wang et al., 1997). One of the subspecies, G. s. marica, is included in the Red Data Book of IUCN (IUCN, 1978, 1992) and another one, G. s. subgutturosa, in the Red Data Book of the USSR (USSR, 1984) and Red Data Books of all the states of the Central Asian part of U.S.S.R., in the limits of its area. In fact the situation in Central Asia is even worse. § Address for correspondence: Dr Antoine Sempere, ´ ´ Villiers en Bois, F-79360, France. ¶ Present address: Bureau CNRS in Moscow, app. 109, 14, ul. Goubkina, 117312, Moscow, Russia. 0140]1963r98r040577q15 $30.00r0
q 1998 Academic Press
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Gazelles inhabit 0.3% of the area they previously occupied in Caucasus and Tadjikistan, and their ranges have been halved in Kazhakstan and reduced even more in Uzbekistan and Turkmenistan (Flint & Prisiadzniuk, 1986). Wildlife in such areas can only be reintroduced if the probable causes of the decline of gazelles are eliminated, and if the group of animals released is numerically strong. To re-establish the goitred gazelle in its native area, special breeding centres were created with the main objective of developing the gazelle population in controlled areas. The first and largest of the centres created in the Middle Asian part of the former Soviet Union was the Bukhara Breeding Centre, Uzbekistan. This centre presents a wide range of conditions, the north being completely arid, and the south having higher biodiversity and some lakes which are connected with the underground water, itself fed by the Amou]Bukhara Canal. Such a range is highly desirable in arid environments where vegetation production is highly dependant on irregular rainfall (Nagy, 1988). This investigation considers the dynamics and adaptation to an arid environment of the present population, which is descended from the founder group of hand-reared animals. Correlation of population growth with seasonal rainfall, in relation to the reproductive cycle (breeding season, gestation, lactation) was investigated to establish the extent to which reproductive success of this population depended on population density andror environmental factors (rain, temperature, food).
Materials and methods This study was conducted in the southern Kyzylkum Desert at the Bukhara Breeding Centre, Uzbekistan (408 N, 658 E) which was established in 1978 with the main purpose of breeding goitred gazelles in intensive husbandry for repopulating their optimum habitat, the desert. The centre comprises fenced territory of 5126 ha, pens and buildings, three observation towers and a system of lakes, connected by a canal and the underground water. The water is saline to the extent of 2 to 17 g ly1 (Prisiadzniuk, 1986) in its southern part. The length of the reserve is about 15 km from the north to the lakes in the south, and it is not wider than 3 km in the middle part.
Climate Meteorological data were obtained from Bukhara airport, 15 km from our reserve. During the 12 years from 1982 to 1994 most precipitation fell between December and May. Annual precipitation ranged from 78 mm (1989) to 245 mm (1993) with a mean ("SEM) of 158 " 10 mm. The dry period lasts from April to November (-20 mm monthy1 ) (Fig. 1). Maximum temperature occurs in July (mean 298C) when the highest daily temperature reaches 408C to 468C (42.5 " 0.48C). It is coldest during December and January, when minimum daily temperature falls to y88C to y258C. Snow is very rare (once in 4]6 years) and fallen snow does not persist.
Vegetation The main zones of vegetation in the breeding centre are: hilly and undulating sandy plain; saline land; and saline lake depression. The plateau (rocky hill) is surrounded by the lower slopes of the main hill. The north of the reserve is mainly sand and gravel plain, whereas lakes are present in the south. There are ten main plant associations (Fig. 2; from Shenbrot, 1987; Mordonov,
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Figure 1. Climatic characteristics 15 km from Bukhara Breeding Centre in 1982]1994. (a) The three lines represent maximum (l), mean (') and minimum ()) monthly temperatures; (b) mean monthly rainfall " SEM. Asterisks indicate significant differences between consecutive months.
1993): riparian forests, with reeds, Phragmites communis, and tamarisk, Tamarix sp.; halophytic communities of the wetter saline lands}Halocnemum strobilaceum, Kalidium spp., Hallostachys caspica, Suaeda spp., Gamantus owimus; plant associations of compressed gypsum sandy loam and loamy soil plains}Zigophyllum spp., Alhagi pseudalhagi, Aelenia spp.; plants of sandy loam and loamy hills}Salsola spp., Reamuria turkestanica; plant associations on the slopes of rocky hills on sandy-gravel loams}Artemisia terrae-albae, A. herba-albae, A. diffusa, Ephedra sp.; gypsophilic plant associations on the rocky tops of hills}Salsola spp., Convolvulus spp., Astragalus spp.; sandy-gravel soil associations on the cones of valleys}Stipa gogenacerii, Calligonum junceum; psammophilic vegetation of the bottoms of valleys}Aristida pennata, Smirnovia turkestana; plants of undulating sandy plains}Ammotamnus
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Figure 2. Plant associations in the Bukhara Breeding Centre: 1 s lakes; 2 s riparian forests (reeds, tamarisk); 3 s halic plants of clay or wet saline lands; 4 s plant associations of compressed gypsum sandy loam and loamy soil plains; 5 s plants of sandy loam and loamy soil hills; 6 s plant associations on the slopes of rocky hills on gravely-sandy loams; 7 s gypsophilic plant associations on the rocky tops of hills; 8 s sandy-gravely soil associations in the cones of valleys; 9 s psammophilic vegetation of the valley bottoms; 10 s plants of undulating sandy plains; 11 s plants of hilly-sandy plains; 12 s plant-free areas. (For the plant associations themselves, see in the text.) 13 s observation towers. A]J, 0]30 s network for mapping animals.
lemanna; and plants of hilly-sandy plains}Salsola spp., Astragalus spp., Convolvulus hammsola, Artemisia diffusa. Cover abundance of the vegetation is 5]75%, and the productivity varies from 190 to 620 kg hay1 (dry weight) depending on the plant association with variation between years. Variation of productivity in one and the same association can vary 4]5 fold between years due to ephemeral vegetation, depending on the humidity and temperature in spring, and local productivity of up to 1279 kg hay1 on the mountain slopes and up to 2186 kg hay1 on the saline-land depression in favourable years has been recorded (Mordonov, 1993).
Animals Forty-four goitred gazelles ( Gazella subgutturosa subgutturosa, Guldenstaedt, 1780) (21 ¨ males and 23 females) aged 1]2 (20%), 3 (40%) and 4]5 (40%) years, were collected and hand reared in different areas of Uzbekistan and were set free on the main territory of the breeding centre in May 1977. Five of them had been injured during transportation, so it is unlikely that they survived very long. The animals were set free 2 km from the buildings of the centre and about 1 km from the main watering places
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(C3, Fig. 2). Within a few weeks of their release into the centre in 1977, the flight distance of the gazelles increased from some dozens of metres to approximately 500 m. Female goitred gazelles in native populations usually become fertile at the age of 18]19 months, but occasionally at 7]8 months, if their weight reaches 16 kg. Males only become fertile at 18]19 months. Breeding takes place from the end of November to mid December, or sometimes till the beginning of January (with some variations in different populations), gestation lasts from 148 to 163 days, and parturition occurs during late April and May. As many as 75% of females in a population may produce twins, although single fawns are typical for the first parturition and for the majority of females in less favourable conditions. The main period of lactation lasts 65 to 80 days, although some fawns continue to suck until October (Geptner et al., 1961; Djevnerov, 1984; Kutcheruk, 1995). In order to determine the size of the population in the centre, censuses have been made yearly in October since 1981 (Flint et al., 1986). (There was no exact census on the growth of the group in 1979]1981; data were obtained just by observations from towers.) The census proceeded as follows: (1) route census in the north part of the centre, observers (7]8 persons) keeping in visual contact with each other while moving along parallel routes from the north border to a line of hides in the middle of the centre; (2) driving animals from the southern part of the centre, about 20 persons moving from the southern border to the north along parallel routes at a distance of 200}250 m from each other; (3) driving animals from the southern part of the centre along the open middle part through the line of hides, with animals passing between hiding places being counted and age and sex noted. During this census, dead animals were recorded. Only two age classes have been distinguished: adults (more than 15 months, potentially reproducers) and fawns (about 5-months-old). Sex is determined easily for adults (only males have horns) but is not possible for fawns during the census. An annual reproductive index was calculated, defined as the number of fawns divided by the number of adult females. This global index includes fecundity, neonatal survival and percentage of reproductive females. The area was divided into three zones: south (up to A7]J10), middle (up to A16]J17) and north. Population densities and animal distribution for each zone were deduced by observations from the three observation towers (Fig. 2) (Flint et al., 1986) and by the density of faeces (Mordonov, 1993). As the fence was not truly repaired for a long time, some occasional emigration of animals occurred beginning in 1984, being registered by density of tracks crossing the border (not exact number of animals, but approximate amount}single, dozens, hundreds).
Statistical analysis All data have been analysed using Simstat 1997. After verification of no correlation between climatic variables, we used step by step multivariate regression analysis to explore the relationships between reproductive index and the following variables (only three of them are explanatory): population density (one variable), bimonthly mean temperature (six variables) and bimonthly number of rainy days (six variables). Growth rate of the population has been assessed by a linear regression of the population size from 1977 to 1989, the period leading to the highest population. Negative residuals appear in 1987, so we have divided the two periods for further comparisons (before and after 1987) assuming a change in population dynamics.
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Table 1. Growth of gazelle population in the Bukhara Breeding Centre from 1977 to 1995
Year
Population
1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995
44 49 71 108 186 271 410 606 580 721 900 1137 1224 1008 814 916 628 712 580
Growth rate
Index of reproduction*
0.114 0.449 0.521 0.722 0.457 0.513 0.478 y0.043 0.243 0.248 0.263 0.077 y0.176 y0.192 0.125 y0.314 0.134 y0.185
0.705 0.86 0.879 0.87 0.97 0.36 0.446 0.607 0.703 0.417 0.27 0.569 0.286 0.508
* Number of fawns divided by number of adult females.
Mann-Whitney tests were used to compare the reproductive indices of the population and fawn proportions within the two periods. Chi-square ( x 2 ) tests were used to compare the density of the populations in the three zones of the reserve during the two periods. Results Population growth From 1977 to 1989, a period of 12 years, the population in the reserve grew from 44 to 1224, and then declined (Table 1, Fig. 3(a)). Until 1989, there was an exponential growth (ln( N ) s 0.3001 x y 19.23, r 2 s 0.9599) with a very high mean coefficient of population growth (1.32 " 0.22; Fig. 3(b)). After 1989 the population tended to ) ) decrease (mean coefficient s y0 .10 " 0 .19 from 1990 up to 1995) (Fig. 3(a-(c)), although variations between years were considerable. However, as early as 1987, growth rate slowed down, regression residuals of ln( N ) s f (year) becoming negative (Fig. 2). This allowed us to divide the period in two: before and after 1987. The reproductive index was high from 1977 to 1986 (Fig. 4). Breeding success was significantly higher between 1982 and 1986, 0.86 " 0.1, than between 1987 and 1994 when it decreased to 0.46 " 0.15 (U s 0, p - 0.01). It corresponds to a mean of 29.8 " 2.6% of fawns in the total population in October before 1987, and 20.3 " 8.1% after 1987. During the whole period of the study (1977]1995), the percentage of animals found dead in the reserve was almost always less than 10%. The causes of mortality are not known. Of the dead animals, 42% were fawns and 58% were adults and sub-adults.
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Figure 3. Development of the gazelle population in Bukhara Breeding Centre from 1977 to 1995 (data of October census). (a) Changes in the number of animals registered during the census; (b) index of population growth in 1977]1989; (c) growth rate of the population ( NxrNxy1 , where N s number of animals registered during the census; x s a year of census, and x y 1 s previous year).
In consequence of the decrease of breeding success beginning in 1986, the percentage of fawns decreased from a mean of 31.2% before 1987 to 17.5% after 1987. The sex ratio of adults remained around 1:1 often with slightly more females (53.9% " 1.1%) from 1987 to 1995 (Fig. 5). This is similar to the sex ratio of the foundation group of animals introduced to the centre (52.3%; 21 male and 23 females). The distribution of the population between the three geographical zones of the centre remained practically stable between 1983 and 1989, keeping the same ratio from
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O. B. PERELADOVA ET AL.
Figure 4. Index of reproduction (fawns per female in October).
the north to the south (1r4r10) ( x 2 test), although the total number of animals increased by three times (from 410 up to 1224). The decrease of population density from the south to the north is closely connected with the heterogeneity of the centre. The mean population density (animals per 100 ha) changed from 40 in 1983 to 123 in 1989 in the southern zone; from 18 to 54 in the central zone; and from 4 to 13 in the northern zone.
Environmental factors Multivariate regression step by step consists of three different explanations of the changes in reproductive index (IR): IR s y3 .5806 q ( 0 .1948 " 0 .06138 = TEMP89 ) q
( y0 .1265 " 0 .0422 = DRF67 ) q ( y0 .0003964 " 0 .000185 = POP ) R 2 s 0 .7150; to enter p s 0 .1; to remove p s 0 .15
Figure 5. Sex ratio of adult animals in the population in October (date of census): ( number of males; (- - - - -) s number of females.
)s
INFLUENCE OF ENVIRONMENT ON GOITRED GAZELLES
585
Table 2. Analysis of the changes in reproductive index
Explanatory variables
Variable
Beta ( b )
Standard error SEM
Origin TEMP89 DRF67 POP
y3.5806 0.1948 y0.1265 y0.000396
0.0614 0.0423 0.00019
Correlation
Partial correlation coefficient
t
p
0.584 y0.3951 y0.4099
0.7268 y0.7064 y0.5809
3.174 2.994 2.141
0.0113 0.0151 0.0609
F
p
7.525
0.008
df.
F
Analysis of variances Source Regression Residual
df. 3 9
Sum of squares Mean square 0.4986 0.1988
0.1662 0.0221
Durbin]Watson test s 1.91 Summary of tests of changes Step 1 2 3
Variable
R2
qTEMP89 qDRF67 qPOP
0.341 0.5698 0.715
Change of R 2 0.341 0.2288 0.1452
1, 11 1, 10 1, 9
p
0 1 5.317 0.0438 4.584 0.0609
TEMP89 s mean temperature in August and September; DRF67 s days with rainfall in June and July; POP s size of the population in October.
where TEMP89 s mean temperature in August and September ( t s 3.521, p - 0.01; F s 12.399, p - 0.01), DRF67 s days with rainfall in June and July ( t s 3.254, p s 0.0116; F s 5.317, p s 0.0438), and POP s size of the population in October ( t s 2.858, p s 0.0212; F s 4.584, p s 0.0609). Variations of the equation are given in Table 2 ( b is a coefficient of a partial regression, which appears in the equation of regression). The step by step multivariate regression analysis proves a strong positive correlation of IR with temperature in August]September, and negative correlation with the number of days with precipitation in June and July and with the size of population. Table 3 presents excluded variables, which do not prove significant correlations with the reproductive index.
Discussion The new gazelle population introduced into the fenced area showed exponential growth from 1977 to 1987, which indicates that the population increased without any restraint. This makes it possible to examine specifically the potential for free growth in this goitred gazelle population, which is even higher (1.44}mean for the period 1977]1987) than in European roe deer (1.32; Gaillard, 1988) and Alpine ibex (1.28; Toıgo ¨ et al.,
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Table 3. Variables with no significant correlation with the reproductive index, rejected from the multivariate regression
Variables* temp 10]11 temp 12]01 drf 10]11 drf 12]01 drf 02]03 drf 04]05 drf 08]09 temp 02]03 temp 04]05 temp 06]07
F
p
0.375 0.188 2.719 1.769 0.019 0.02 1.471 0.001 0.361 0.093
0.5554 0.6748 0.1336 0.2162 0.8947 0.8896 0.256 0.9703 0.5626 0.767
* temp 10]11 s mean temperature of October]November, etc.; drf 02]03 s number of days with rainfall in February]March, etc.
1997) which are known to be the most efficiently reproducing wild ruminant species in Europe, and higher than the mountain gazelle of Saudi Arabia (1.32) which has two reproductive periods a year yielding a single fawn (Dunham, 1997). The phase of exponential growth from 1977 to 1983 coincided with occupation of the south zone of the Centre, and subsequently to occupation of the central and northern zones, which are ecologically less favourable for the animals (mainly due to absence of watering). The southern zone, being the most humid and thus the most rich in vegetation, supports the highest population density. Occupation of the whole area has been advancing step by step. The proportion of the population in each zone, reflecting ecological conditions, had remained stable through the years and at different absolute population densities. The population density in the south continued to grow until 1989 as the carrying capacity was not fully utilized. Emigration of animals since 1984 would correspond to the natural behaviour of spacial dispersion, and the high population density would amplify this phenomenon (Johst & Brandl, 1997). The level of population growth itself should be interpreted very carefully, taking into consideration different factors. It may be suggested that the population decrease after 1989 was connected with both emigration and with declining reproductive success (fertility of adults and survival of fawns). Mordonov (1993) interprets the seasonal disappearance of plant species preferred by gazelles from some places in 1989 (Prisiadzniuk & Soldatova, 1984) as a sign of overgrazing. Our results indicate an overstocking of the area (high number of animals, low reproductive index). Due to the decrease of breeding success and population growth since 1986, we suggest that the effect of population density was cumulated within the 3 years before 1989. This phenomenon may not have been limited to the southern zone. Although the population density, which was regularly checked by counting the amount of faeces (Mordonov, 1993), continued to grow, the proportion in each zone continued to be 1r4r10 in both 1983 and 1989 in favour of the south. If overpasturing took place only in the south, the proportion could change in favour of the north. This was not the case, so it is probable that the low amount of available vegetation in the north, combined with the long distances to watering places, could be a limiting factor for population density in the north. In any case, the stable proportion 1r4r10 indicates a parallel increase in pressure on available vegetation in all zones. Population density in the southern and central zones became higher than has been registered for mountain gazelles (15 gazelles 100 hay1 ) (Dunham, 1997), due to better
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food and water resources in these parts of the Centre. In the north it is different; here the local density does not reach those observed in Saudi Arabia, and is never higher than 12.8 gazelles 100 hay1 . It can thus be concluded that all the area of the reserve has been utilized since 1983 (equivalent proportion of local densities) and overexploited (negative residuals of regression, see above) since 1986. The recorded sex ratio of the population could be slightly biased in favour of females, as sub-adult males are often counted as females during the census. But still it remains around 1.17 females:1 male (see Fig. 5), which is similar to the proportion of the initially introduced group (1.1:1), and more equal than the reintroduced population of mountain gazelles in Saudi Arabia (1.6:1) (Dunham, 1997). The presence of a nearly equal number of males (who are utilizing the food resources) is not useful for the reproductive success of the population, and it increases the density-dependence of the population. In the population of mountain gazelles studied by Dunham, only 45% of males were territorial (that is reproductive), and so the corrected sex ratio for reproductive animals was 3.6:1, similar to the results obtained with other Antilopinae (4:1; Jarman, 1974; Wang et al., 1997). Similarly, we suggest that the high percentage of bachelor males andror non-territorial and opportunist reproductive males (Marmosinskaia, 1996) is very important for the dynamics of the population. Fluctuations of the number of animals around some optimum and sex ratio regulation can be achieved in populations in different ways. One of them, which is very important for open populations in nature, is emigration. In the Bukhara population this could play a part (Marmosinskaia, 1996; Soldatova & Bahloul, pers. obs.) because the enclosing fence had been damaged on occasion even before 1989, and was not regularly repaired. So emigration of young males since 1989 may have contributed substantially to the decline of the population. During the breeding season (November to December), male gazelles control their harem, moving around with it, when population density is low; when population density is high some males become territorial and participate in reproduction, while others remain mobile in non-reproductive bachelor groups (Mambetdjumaev, 1970; Gorelov, 1972; Djevnerov, 1984; Blank, 1985). In the Centre, territorial behaviour of males in November and December has been noted since 1985, at least in the southern part, and all over the Centre later (Marmosinskaia, 1990). This social interaction could therefore cause emigration (to the north and outside of the Centre), mainly of bachelors, from reproductive areas during the period of territorial behaviour. This kind of regulation of the male population could be beneficial for the breeding activity of the adult population, decreasing grazing pressure and the level of competition between males, and so reducing losses of energy of territorial males participating in reproduction and subsequent mortality level (Ralls et al., 1980; Promislow, 1992). The high percentage of fawns before 1987 (29%), which was similar to that recorded in the wild for Mongolian gazelles (Wang et al., 1997) and in introduced mountain gazelles (42%) (Dunham, 1997), seriously decreased after 1987 (20%). Interactions between females in the high-density population might have inhibited ovulation and consequently fertility (Alados & Escos, 1992). Moreover it may be that the presence of a high proportion of young adult females (connected with the rapid growth of the population during previous years), which are less productive than multiparous females, at least in related species (Olmedo et al., 1985; Alados & Escos, 1991; Langvatn et al., 1996), affected breeding success and therefore the percentage of fawns. At Bukhara two periods of vegetation growth are usually observed, in spring and autumn, with a quiescent period in summer. The best development of vegetation was observed in autumn, while 50% of living parts of plants was grazed in spring (Mordonov, 1993). Summer rain has a negative effect on the survival of fawns aged from 1- to 4-months-old, despite the increase of plant growth that occurs with high
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precipitation in an arid environment (Nagy, 1988). Some data indicate that thermoregulation in fawns is poor during the first month of life (Hull, 1973). According to our observations in 1996]1997 numerous animals were found dead in the Centre after heavy late spring and early summer rains. Moreover, according to previous investigations in pens at another breeding centre, there is a category of fawns that is exceptionally at-risk to die after rain (Pereladova, 1986). This could result from the effect of rainfall on heat loss, mainly during the night when there is a sharp fall in temperature, as has also been shown for sheep (Webb et al., 1984). In fact, rainy days in June and July can slightly reactivate the vegetation, which is usually absolutely dry in July and August, and consequently reduce the autumn forage production, which corresponds to the weaning period and the highest food requirements for the fawns. Moreover, summer rains encourage development of parasites, mainly in fawns (Masson, 1977), and can reduce or stop lactation further adversely affecting survival of fawns. Dry months (August and September) have a positive effect on breeding success (survival of fawns) and this is surprising after 3 months of dryness. High temperatures in early autumn stimulate vegetation growth (even without rains) and also delay the approach of winter. It should be especially emphasized that the intermediate seasons (autumn) are rather short in a continental climate and are challanging to animals. So, the occurence of a ‘prolonged’ summer allows fawns to achieve a body condition that is adequate (compensatory growth after weaning; Albon & Clutton-Brock, 1992; Andersen & Linnell, 1997) to allow survival during the early (November) and rather cold winters of the continental climate, by aiding thermoregulation of fawns at the beginning of the cold period. Population density (Table 2) has a low negative effect on breeding success. This was evident during the first period after introduction (1977]1983) when there was no density dependence (Johst & Brandl, 1997). Afterwards, an indirect effect of population density (limitation of food) could possibly affect the body condition of females and delay oestrus and so affect the survival of fawns in the next autumn (White, 1990). Lack of sensitivity of our index of reproduction could explain the relative independence of breeding success from density. Different components of the reproductive index (fecundity, neonatal mortality, post-weaning mortality) can compensate their individual variations, reducing the overall variation of the reproductive index induced by density ( Allaine ´ et al., 1992) . It seems that spring precipitation had no positive influence on breeding success, probably because of the low dependence of the vegetation in the southern part on rainfall, in contrast to that observed in the Arabian Desert (Dunham, 1997). Vegetation growth at Bukhara is more dependent on changes in the level of underground water and lakes inside the reserve which is artificially controlled by the level of the Amou]Bukhara Canal. Thus the amount of vegetation needed for normal lactation of gazelles in the first month is not dependant on rains in the most densely inhabited southern zone.
Conclusion Our investigations have shown that the breeding success of goitred gazelles in the Bukhara reserve is correlated with meteorological conditions (i.e. late spring rainfalls had a negative effect, while high autumn temperatures had a positive effect on body condition of fawns) and is density dependent. This preliminary study was made because this species, endogenous to Central Asia, must adapt to water restraint, as must African ungulates, and also to seasonally cold conditions of paleoarctic species. None of the existing theories on the growth of
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populations in an arid environment, which have been developed mainly on African models (living without cold seasons), could be utilized in our case. There have been studies on the ecology of populations of this type but because they have been published in Russian they are not widely known or used in the development of such theories. On the other hand, there are Russian works which develop theories of population dynamics, but deal with populations in forest and steppe zones, which are different in principal from arid conditions in continental deserts. So we could not use these theories either for interpreting our data on population development. Thus these original data can form the base for future development of a theoretical model. Another important conclusion is that the choice of reintroduction conditions (ecological conditions, size and sex ratio of the initial group, which define the growth of the group during the first phase of growth) may lead to a durable population structure, which does not necessarily correspond to a stable natural population (sex ratio, migration rate, breeding success). We are very grateful to the Ministry of Ecology of Uzbekistan, ‘Gosbiocontrole’, Mr A.K. Atadjanov and the Directors of the Bukhara Breeding Centre, for enabling our work to take place. We give special thanks to Natasha Marmosinskaia, Bakhtiour Mordonov and other staff of the Centre for collecting data and for participating in the census. We thank the specialists of the All-Russia Research Institute of Nature Conservation, led by Prof. V.E. Flint, for their help and participation in our work. We are also grateful to Dr J.M. Gaillard and Prof. H. Barre ´ for comments and corrections on statistical data, and the reviewers for their constructive comments. This analysis made possible by a grant from CNRSrMAE PICS 266. We thank Dr S.J.G. Hall for help in improving the manuscript.
References Alados, C.L. & Escos, J.M. (1991). Phenotypic and genetic characteristics affecting lifetime reproductive success in female Cuvier’s, dama and dorcas gazelles ( Gazella cuvieri, G. dama and G. dorcas ). Journal of Zoology, London, 223: 307]321. Alados, C.L. & Escos, J.M. (1992). The determinants of social status and the effect of female rank on reproductive success in dama and Cuvier’s gazelles. Ethology, Ecology and Evolution, 4: 151]164. Albon, S.D. & Clutton-Brock, T.H. (1992). Cohort variation in reproduction and survival: implications for population demography. In: Brown, R.D. (Ed.), The Biology of Deer, pp. 15]21. Berlin, Heidelberg, New York: Springer. 596 pp. Allaine, ´ D., Houssin, H. & Gaillard, J.M. (1992). Etude de la variabilite´ spatio-temporelle d’un indice de reproduction dans une population de chamois ( Rupicapra rupicapra). Gibier Faune Sauvage, 7: 85]94. Andersen, R. & Linnell, J.D.C. (1997). Variation in maternal investment in a small cervid; the effects of cohort, sex, litter size and time of birth in roe deer ( Capreolus capreolus ) fawns. Oecologia, 109: 74]79. Blank, D.A. (1985). Specificity of social and reproductive behaviour of gazelles ( Gazella subgutturosa) in the valley of Ili river. Zoologitcheskii Journal, 64: 1059]1070. (In Russian.) Djevnerov, V.V. (1984). Goitred Gazelle of Barsakelmes Island. Alma-Ata: Nauka. 144 pp. (In Russian.) Dunham, K.M. (1997). Population growth of mountain gazelles reintroduced in central Arabia. Biological Conservation, 81: 205]214. Flint, V.E. & Prisiadzniuk, V.E. (1986). Population condition, conservation and future of goitred gazelle restoration in the USSR. In: Flint, V.E. & Prisiadzniuk, V.E. (Eds), Conservation and Future Restoration of Goitred Gazelles in the USSR, pp. 3]8. Moscow: Gosagroprom. (In Russian.) Flint, V.E., Prisiadzniuk, V.E. & Soldatova, N.V. (1986). Bukhara breeding centre. Information
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4. Goitred gazelle census. In: Flint, V.E. & Prisiadzniuk, V.E. (Eds), Conservation and Future Restoration of Goitred Gazelles in the USSR, pp. 43]49. Moscow: Gosagroprom. (In Russian.) Gaillard, J.M. (1988). Contribution `a la dynamique des populations de grands mammiferes: ` l’exemple du chevreuil ( Capreolus capreolus ). Ph.D. thesis, University of Lyon, France. 308 pp. Geptner, V.G., Nasimovitch, A.A. & Bannikov, A.G. (1961). Mammals of the Soviet Union, Vol. 1, Ungulates. Moscow, High School. 714 pp. (In Russian.) Gorelov, J.K. (1972). Reproduction of goitred gazelles and the problem of its restoration in Badhis. Theriology, 1: 420]424. (In Russian.) Hull, D. (1973). Thermoregulation in young mammals. In: Whitton G.C. (Ed.), Comparative Physiology of Thermoregulation, pp. 167]200. IUCN (1978). Red Data Book of International Union for the Conservation of Nature, Vol. 1. Switzeland: Merdges. IUCN (1992). Red Data Book of International Union for the Conservation of Nature, Vol. 1. Switzeland: Merdges. Jarman, P.J. (1974). The social organisation of Antilope in relation to their ecology. Behaviour, 48: 215]267. Johst, K. & Brandl, R. (1997). Evolution of dispersal: the importance of the temporal order of reproduction and dispersal. Proceedings of Royal Society of London B, 264: 23]30. Kutcheruk, V.V. (1995). Goitred gazelles. In: Kutcheruk, V.V. (Ed.), Mammals of Turkmenistan, Vol. 1, Predators, Pinnipedia, Ungulates, pp. 222]237. Ashgabad: Ilym. (In Russian.) Langvatn, R., Albon, S.D., Burkey, T. & Clutton-Brock, T.H. (1996). Climate, plant phenology and variation in age of first reproduction in a temperate herbivore. Journal of Animal Ecology, 65: 653]670. Mambetdjumaev, A. (1970). Goitred Gazelles. Tashkent, Fan. 196 pp. (In Russian.) Marmosinskaia, N.V. (1990). Social behaviour of goitred gazelles during the reproductive period. V Congress of All-Union Theriological Society, Abstracts, 3: 32]33. (In Russian.) Marmosinskaia, N.V. (1996). Territorial and marking behaviour of goitred gazelles (Artiodactyla, Bovidae) in Bukhara breeding centre. Zoological Journal, 75: 142]156. (In Russian.) Masson, P.C. (1977). Gastrointestinal parasitism in red deer. New Zealand Journal of Agricultural Science, 11: 182]183 Mordonov, B.K. (1993). Goitred gazelle influence over the vegetation of deserts. Ph.D. thesis, Institute of Nature Conservation, Moscow. 26 pp. (In Russian.) Nagy, K.A. (1988). Seasonal patterns of water and energy balance in desert vertebrates. Journal of Arid Environments, 14: 201]210. Olmedo, G., Escos, J. & Gomendio, M. (1985). Reproduction de Gazella cuvieri en captivite. ´ Mammalia, 49: 501]507. Pereladova, O.B. (1986). Individual specificity of social behaviour of goitred gazelles. In: Flint, V.E & Prisiadzniuk, V.E (Eds), Conservation and the Future Restoration of Goitred Gazelle Number in the USSR, pp. 74]84. Moscow: Gosagroprom. 223 pp. (In Russian.) Prisiadzniuk, V.E. (1986). Bukhara Breeding Centre. Information 5. Watering places of goitred gazelles. In: Flint, V.E & Prisiadzniuk V.E (Eds), Conservation and the Future Restoration of Goitred Gazelle Number in the USSR, pp. 59]70. Moscow: Gosagroprom. 223 pp. (In Russian.) Prisiadzniuk, V.E. & Soldatova, N.V. (1984). Bukhara Breeding Centre. Information 1. Foraging of goitred gazelles in semi-wild conditions in sandy hills. In: Scientific Basis of Conservation and Sustainable Usage of Animals World, pp. 28]43. Moscow: VNII priroda. 275 pp. (In Russian.) Promislow, D.E.L. (1992). Cost of sexual selection in natural populations of mammals. Proceedings of the Royal Society of London B, 247: 203]210. Ralls, K., Brownwell, R.L. & Ballou, J. (1980). Differential mortality by sex and age in mammals. Report of the International Whaling Commission, Special issue, 2, pp. 223]243. Red Data Book of the USSR (1984). Moscow: Lesnaja promishlennost. 72 pp. (In Russian.) Shenbrot, G.I. (1987). The productivity of pastures and the role of rodents as food competitors of gazelles. In: Regional Aspects of Gazelle’s Biology. VINITI, 2745-B87, Moscow, pp. 105]113. (In Russian.) Toıgo, ¨ C., Gaillard, J.M. & Michallet, J. (1997). Adult survival pattern of the sexually dimorphic Alpine Ibex ( Capra ibex ibex ). Canadian Journal of Zoology, 75: 75]79
INFLUENCE OF ENVIRONMENT ON GOITRED GAZELLES
591
Wang, X., Sheng, H., Bi, J. & Li, M. (1997). Recent history and status of the Mongolian gazelle in Inner Mongolia, China. Oryx, 31: 120]126. Webb, D.R., Dineen, J.K. & Kelley, J.D. (1984). Effects of wetting on insulation of bird and mammals coats. Journal of Thermal Biology, 9: 189]191. White, G.R. (1990). Nutrition in relation to season, lactation, and growth of north temperate deer. In: Brown R.D. (Ed.), The Biology of Deer, Proceedings of International Symposium on the Biology of Deer, Mississippi, 28 May]1 June 1990, pp. 407]417. New-York Inc: Springer-Verlag. 596 pp.