Restoration of Chlamydotis undulata macqueenii (Houbara Bustard) Populations in Saudi Arabia: A Progress Report

During the last two decades Chlamydotis undulata (houbara bustard) has declined drastically throughout its range, due primarily to over-hunting and severe habitat degradation. The threatened extinction of local populations led the National Commission for Wildlife Conservation and Development of Saudi Arabia to implement ex- and in-situ conservation measures: (1) a captive breeding program initiated in 1986, which achieved production of a self-sustaining breeding flock as well as a surplus for reintroduction by 1992; (2) establishment of a 13,775-km2 protected area around the last known breeding population in Saudi Arabia; (3) studies of wild birds, to determine densities, feeding ecology, and habitat requirements; and (4) studies on different release techniques (adult releases, sub-adult releases, feather-cut sub-adult releases, and covey releases), carried out since 1991 within the 2,300-km² fenced and protected area of the Mahazat as-Sayd reserve.     

Seasonal changes in habitat use by Houbara Bustards Chlamydotis [undulata] macqueenii in northern Saudi Arabia

Habitat preferences by Houbara Bustards Chlamydotis [undulata] macqueenii in Harrat al-Harrah reserve, in northern Saudi Arabia were determined from sightings of birds in all seasons over three years. Vegetation and crawling invertebrate abundance were sampled in each habitat. Houbara Bustards showed seasonally changing habitat preferences that appeared to be influenced primarily by vegetation phenology, abundance and cover. More densely vegetated areas (10–17% cover) were preferred. Seasonal and inter-habitat variations in invertebrate numbers were not reflected in differential habitat use by Houbara Bustards. The highest selection ratio for a single habitat (dry lakes) occurred in summer, coinciding with the fruiting of Shafallah Capparis spinosa. Selectivity of habitats was least in spring, when green vegetation was most widespread. Changes in Houbara Bustard habitat preferences in response to marked seasonal changes in habitats brought about by well-defined patterns of rainfall indicate that studies of habitat selection should consider the entire annual cycle. The importance of vegetative cover and the sensitivity of Houbara Bustards to human disturbance suggest that reserves set aside for Houbara Bustards should be extensive, diverse and largely free of livestock, human occupation and its associated disturbances.     

Breeding success in a Houbara Bustard Chlamydotis [undulata] macqueenii population on the eastern fringe of the Jungar Basin, People's Republic of China

Nesting success and chick survival of a migratory population of Houbara Bustard Chlamydotis [undulata] macqueenii were studied during three consecutive years (1998–2000) in the Xinjiang province of north‐west China. A total of 45 nests was monitored and 85 broods comprising 227 chicks were captured, of which 82 chicks were radio‐tracked. Start of laying varied between 6 and 17 April between years but the laying mode fell consistently between 26 and 30 April. Mean clutch size was 4.0 (sd = 0.8) (range 2–6) for early clutches and 3.3 (sd = 1.1) for late clutches (range 2–5). The average nesting success was 0.588 (sd = 0.270) but great variations were observed between years –0.882 in 1998, 0.530 in 1999 and 0.351 in 2000. This was related to increased predation in 1999 and 2000, which is reflected by increased predator density (chiefly Corsac Fox Vulpes corsac and Long‐legged Buzzards Buteo rufinus). The overall hatchability, defined as the proportion of eggs hatched in successful nests was 0.839 sd = 0.238). The average brood size at hatching varied from 2.9 (sd = 0.8) to 3.3 (sd = 0.9) according to years, and no significant decrease in brood size was observed in the first 5 days post‐hatching. In 1999 and 2000 the brood size diminished sharply (14% and 27%, respectively) in prefledging chicks. A further severe decrease (37%) was observed in fledglings in 2000, probably due to predation by raptors. For the 3 years of the study, a successful female Houbara would bring on average 2.3 (sd = 0.9) chicks to fledging and would have lost 30.2% (sd = 14.9%) of its brood to adversity during the rearing process. The proportion of females that lost their entire brood was 0.181 in 1998, 0.708 in 1999 and 0.453 in 2000. For the 3 years of the study, only 55.3% (sd = 26.3%) of the females hatching eggs brought chicks to fledging. The overall chick production was 0.827 per breeding female per year and the probability of an egg laid producing a fledgling of 8 weeks old was 0.190.     

新疆木垒波斑鸨营巢成功率的初步研究

1998年 4月中旬～ 7月中旬 ,对分布于新疆木垒的波斑鸨 (Chlamydotisundulatamacqueenii)种群的营巢成功率进行了初步考察与研究。考察中共发现 16个巢、2 5窝幼雏。每巢产卵 3～ 6枚 ,卵鲜重 (6 4 7± 5 8)g ,卵径为 6 0 9mm× 43 9mm。产卵有两个高峰期 ,表明雌鸟第 1次繁殖失败后可再次产卵。第 1产卵期的巢卵数为(4 1± 0 8)枚 ,第 2产卵期的巢卵数为 (3 5± 0 6 )枚。雌鸟营巢成功率为 77 5 %～ 87 5 % ,卵的孵化率为83 6 %。每窝内从破壳到具备飞行能力的幼雏数基本不变 ,表明繁殖雌鸟大都能将幼雏全部抚育到可以飞行的年龄     

新疆木垒波斑鸨卵的孵化温度及雌鸟孵化行为的初步研究

1999年 5月 2 2日到 6月 11日 ,在新疆木垒波斑鸨分布区利用装有温度记录仪的假卵成功地监测了2只雌性波斑鸨 (Chlamydotisundulatamacqueenii)的繁殖行为。研究表明 :在孵化期 ,雌鸟的日活动节律呈现出双峰模式 ,即晨昏活动。雌鸟平均每天离巢 3～ 9次 ,每次 8～ 2 6min。孵化过程中 ,雌鸟每天花费 (94±2 ) %的时间孵卵。当雌鸟孵卵时 ,卵的日均孵化温度为 31 9～ 36 5℃。当雌鸟离开巢时 ,卵的温度平均下降到(2 4 9± 3 2 )℃。随着孵化的进行 ,卵的日均温从 31 9℃上升到 36 2℃ ,与环境温度的变化呈正相关。     

Taxonomy of the Houbara Bustard Chlamydotis undulata subspecies considered on the basis of sexual display and genetic divergence

The Houbara Bustard Chlamydotis undulata is a polytypic species with three subspecies classified according size, colour and distribution: C. u. undulata, C. u. fuertaventurae and C. u. macqueenii. A comparative study of the male display behaviour of these three subspecies has shown similarities between C. u. undulata and C. u. fuertaventurae , whereas appreciable differences exist in the visual and auditory aspects of the display between C. u. undulata and C. u. macqueenii. These observations make the current taxonomy of Houbara Bustard questionable, particularly in view of the major importance of the sexual display in bird speciation processes. Furthermore, DNA analysis of the cytochrome b gene indicates the existence of a significant differentiation between the C. u. undulata and C. u. macqueenii populations. These findings indicate the need for a revision of the taxonomy of genus Chlamydotis which should separate the macqueenii and undulata populations at species rank. Until further investigations are completed, C. u. fuertaventurae should be kept as a subspecies of undulata since the courtship display is alike in both populations.     

Relationships between home-range size, sex and season with reference to the mating system of the Houbara Bustard Chlamydotis undulata undulata

This paper presents observations of Houbara Bustard Chlamydotis undulata undulata home-range, in the semi-desert steppe of eastern Morocco. Home-ranges were calculated from radiotagged birds using the fixed kernel method (LSCV). The mean annual home-range of males (17 km²) was smaller than that of females (146 km²; P  < 0.001). The majority of male home-ranges had a unimodal distribution (86%), whereas 67% of female home-ranges were multimodal. Consequently, the amplitude of female movements was larger (mean: 44 km/13 km; P  < 0.002). In spring, male home-ranges decreased in size around display sites (8 km²) and many of them overlapped considerably. Display sites show an aggregative distribution ( P <  0.001) and a single female reproductive range may contain the display sites of several males. The data fulfil the definition of an exploded lek social structure. In our study, C. u. undulata appears to be sedentary with relatively limited home-ranges. Successive years of fidelity to home-ranges indicate that adults are not nomadic.     

Characterization of 22 microsatellites loci from the endangered Houbara bustard (Chlamydotis undulata undulata)

Here we present a new set of 22 microsatellite loci isolated from Chlamydotis undulata undulata, an endangered Houbara bustard found across North Africa. The number of alleles per locus ranged from one to nine, and heterozygosities ranged from 0.167 to 0.944. Total exclusionary probabilities using these loci for the first and the second parent were 0.992932 and 0.999915, respectively. Successful cross‐amplification was observed in eight other Otididae species (12–22 of the 22 loci). These microsatellite markers are powerful tools for genetic identification, paternity assignment and population genetic studies.     

Variability in the size of the nucleus in spermatozoa from Houbara bustards, Chlamydotis undulata undulata

Semen collected from 3-year-old male Houbara bustards contained large proportions (6-40%) of spermatozoa with large nuclei. In these spermatozoa, the length of the nucleus was up to twice the mean length of the nucleus in normal spermatozoa. The lengths of the acrosome, midpiece and flagella were all normally distributed, but the length of the nucleus formed a bimodal distribution. The proportion of spermatozoa with large nuclei varied among males, but not among different semen samples collected from the same male throughout the breeding season. The proportion of motile spermatozoa with large nuclei was half that of normal spermatozoa, but their velocity was significantly greater. After insemination into females, spermatozoa with large nuclei were observed in the outer perivitelline layer of eggs laid, indicating that they were stored and transported within the oviduct and reached the egg at about the time of fertilization. Furthermore, there was no difference in the ability to produce viable progeny in females that were mated with males producing greater proportions of spermatozoa with large nuclei compared with those producing 'normal' spermatozoa. Thus, the abnormal spermatozoa did not appear to impede fertility. There were no signs of triploidy in the males that produced spermatozoa with large nuclei, or in their progeny, as demonstrated by the size of erythrocytes. Therefore, it appears that the spermatozoa with large nuclei were the result of aberrant spermatogenesis.     

Migration and range use of Asian Houbara Bustard Chlamydotis macqueenii breeding in the Gobi Desert, China, revealed by satellite tracking

Four adult male Asian Houbara Bustards Chlamydotis macqueenii were caught on their breeding grounds in the Gobi Desert of China and tracked by satellite from July 2000 for from 5 months to > 3.5 years. Wintering areas were identified for two individuals, one on the Turkmenistan/Uzbekistan border in the Amur-Darya valley, the second at the Iran/Turkmenistan border. One individual used the same wintering and breeding areas for three consecutive years. Overall departure dates from breeding grounds ranged from 29 September to 14 October, with arrival on wintering quarters from 23 October to 7 November. Birds left their wintering grounds between 2 and 21 March and reached their breeding areas between 11 and 21 April. The mean overall migration distance was 3935 km (sd = ± 229, n  = 9). Houbara Bustards mainly followed steppe areas to migrate avoiding the highest elevations of the Himalayan massif and travelling 267 km/day on average. Pre-breeding migration lasted longer than post-breeding and included more and longer stopovers. The Taukum Desert and Jungar Basin are critical areas for migration of eastern Houbara populations. Breeding range, used for 5.5 months, was 274 km² (sd = ± 53, n  = 4), whereas wintering range, used for around 4 months a year, was 76 km² (sd = ± 22, n  = 3). Range use pattern appeared similar for Asian Houbara released in central Saudi Arabia, but differed from the African Houbara Bustard. More investigations are required to determine the effects of food availability and meteorological conditions on the migration pattern and on the use of stopovers by Asian Houbara Bustards.     

Survival rates of captive‐bred Asian Houbara Chlamydotis macqueenii in a hunted migratory population

Asian Houbara Chlamydotis macqueenii numbers are declining as a result of unsustainable levels of hunting and poaching, with the main conservation response being population reinforcement through the release of captive‐bred birds. We assessed the contribution of captive breeding to the species’ conservation by examining the fates of 65 captive‐bred birds fitted with satellite transmitters and released during spring (March–May) and autumn (August) into breeding habitat in Uzbekistan. Of the released birds, 58.5% survived to October, the month favoured by Emirati hunters in Uzbekistan, but only 10.8% of those released survived the winter to return as subadults next spring. To mitigate and compensate for the loss of wild adults to hunting, the number of released birds needs to be an order of magnitude higher than hunting quotas (with a release of between 1640 and 1920 required for a hypothetical quota of 200), indicating that releases may be costly and do not remove the need for a biologically determined sustainable hunting quota.     

Peptidergic and aminergic neurotransmitters of the exocrine pancreas of the Houbara bustard (Chlamydotis undulata)

The immunochemical distribution of peptidergic and aminergic neurotransmitters in the exocrine pancreas of the Houbara bustard, Chlamydotis undulata, was determined. Immunoreactivity to choline acetyltransferase (ChAT), vasoactive intestinal polypeptide (VIP), and galanin (Gal) occurred mainly as varicose terminals in the walls of capillaries around the acini and arterioles within the connective tissue. Neuronal cell bodies immunoreactive to ChAT were infrequently observed. Neuropeptide Y (NPY), pancreatic polypeptide (PP), and somatostatin (Som) were observed mainly in intra-acinar cell bodies but nerve fibers immunoreactive to these neuropeptides were also seen along the basal surfaces of the acini. Immunoreactivity to NPY and PP was also discernible in cells of the pancreatic ducts. In addition, NPY occurred as varicose terminals in vessels around the ducts. SP occurred rarely in interacinar ganglia. The distribution of tyrosine hydroxylase (TH) was similar to that of ChAT and, in addition, the occasional TH immunoreactive intra-acinar neuronal cell body was observed. Neuronal nitric oxide synthase (nNOS) occurred in neuronal cell bodies among the acinar cells as well as nerve fibers along the bases of the acini. The potential roles of these peptidergic and aminergic neurotransmitters in the neurohormonal control of pancreatic secretion are discussed.     

新疆木垒波斑鸨的繁殖成功率

作者于 1998～ 2 0 0 0年 4～ 7月 ,采用野外直接观察、栖息地植被样方调查和无线电跟踪等方法对分布于新疆木垒的波斑鸨 (Chlamydotiundulatamacqueenii)种群的繁殖生态进行了初步观察与研究。考察中共发现45个巢、 84窝幼雏。研究结果表明 ,木垒波斑鸨有两个产卵高峰期 ,表明雌鸟第一次繁殖失败后可能再次产卵。雌鸟营巢成功率平均为 0 5 0 5。波斑鸨的窝卵数在 2～ 6枚之间 ,出现 4枚卵的频率最高。第一产卵期内的平均窝卵数 ( 4 0± 0 8枚 /窝 )大于第二产卵期内的平均窝卵数 ( 3 3± 0 8枚 /窝 )。木垒波斑鸨种群三年间卵孵化率分别为 0 84、 0 80和 1,繁殖成功率为 0 45 6。种群在繁殖期几乎不受人类活动干扰 ,巢卵及幼雏损失主要来自天敌捕食 ,如沙狐、大和棕尾等.     

Genetic variation across the current range of the Asian houbara bustard (Chlamydotis undulata macqueenii)

The houbara bustard (Chlamydotisundulata), the main quarry for Arab falconry,is currently threatened by excessive huntingand poaching as well as by habitat loss andfragmentation. We have investigated the geneticdiversity, population structure and demographichistory of houbara bustards across theirgeographical range by analyzing mitochondrial(mt)DNA sequences (a 370 bp fragment of controlregion I and a 264 bp fragment of thecytochrome b gene) and 4 microsatelliteloci in 74 individuals sampled from the CanaryIslands to China. Both markers revealed low tomoderate diversity that could be partitionedinto two monophyletic groups or evolutionarysignificant units belonging to the NorthAfrican (C. u. undulata) and Asian (C. u. macqueenii) subspecies. A history ofrelatively recent population growth (35,000years ago) accompanied by range expansion isthe most likely demographic scenario for theAsian subspecies. In addition, Macqueen'sbustards are able to disperse efficiently overbroad areas, which is consistent with ourinference of weak phylogeographic structure(global F _ST = 0.20 and 0.04 formtDNA and microsatellites, respectively) andhigh levels of homogenizing gene flow on widegeographical scales. We therefore suggest thatmanagement actions should focus on maintainingmigratory connectivity between breeding andnon-breeding areas.     

Absence of male reproductive skew,along with high frequency of polyandry and conspecific brood parasitism in the lekking Houbara bustard Chlamydotis undulata undulata

Behavioural studies have led to the perception that lekking species experience a high male reproductive skew as a consequence of females’ selective mate choice. In addition, observations suggest that females copulate only once and therefore polyandry seems unlikely as females are supposed to choose the best male available. In order to analyse the mating strategy of the Houbara bustard, an endangered lekking species under reinforcement in eastern Morocco, we used microsatellite data to perform paternity analyses. None of our observations followed common expectations under a lek mating system: we found no male reproductive skew suggesting no apparent selective female mate choice and no apparent male benefit from lekking. In contrast, a high level of polyandry (60 % of the nests) was recorded suggesting that sperm competition may operate. In addition, we present another case of conspecific brood parasitism in a lekking species and this was an unexpected alternative strategy for a species presenting high parental cost and low fecundity. The increasing number of studies contradicting common assumptions on lekking species suggests that alternative breeding strategies such as males pursuing an off‐lek mating strategy, female polyandry and even conspecific brood parasitism might be more widespread in lekking species than previously thought.     

Neurotransmitters regulating acid secretion in the proventriculus of the Houbara bustard (Chlamydotis undulata): a morphological viewpoint

Endocrine cells containing somatostatin (Som), gastrin-releasing peptide (GRP), and neuronal nitric oxide synthase (nNOS) and nerve fibers containing choline acetyl transferase (ChAT), tyrosine hydroxylase (TH), galanin (Gal), substance P (SP), and vasoactive intestinal polypeptide (VIP) were immunolocalized in the proventriculus of the Houbara bustard, Chlamydotis undulata. While GRP-immunoreactive (GRP-IR) cells occur in the inner zone, somatostatin (Som-IR) and polyclonal nNOS (nNOS-IR) immunoreactive cells were localized mainly in the peripheral zone of submucosal glands. GRP-IR, Som-IR, and nNOS-IR cells were occasionally observed in the walls of the gastric glands. Endocrine cells are of the closed variety and usually possess apical processes extending along the basal surfaces of adjacent nonreactive cells. Ultrastructural features of these cells are typical. ChAT, Gal, SP, VIP, and TH were immunolocalized in nerve fibers and terminals in the walls of arterioles and capillaries at the periphery of submucosal glands. Immunoreactivity to monoclonal nNOS occurred mainly in neuronal cell bodies in ganglia located around the submucosal glands. ChAT and TH immunoreactive cell bodies were also occasionally seen around the submucosal glands in the peripheral region. Immunoreactivity to Gal, SP, and VIP, but not ChAT or TH, was discernible around the walls of gastric glands. It was concluded that the distribution of neurotransmitters in neuronal structures is similar, but that of the endocrine cells varies from that of some avian species. The roles of these neurotransmitters in the regulation of acid secretion are discussed.     

Genetic variability characterization of the moroccan houbara bustard (Chlamydotis undulata undulata) inferred from pedigree analysis

A Moroccan Houbara Bustard pedigree was analyzed to evaluate the genetic variability in captive breeding population using genealogical approaches. The whole Houbara breeding flock (WP) for the period 1993–2004 was made up of 531 birds comprising 346 females and 185 males. The reference population (RP) comprised 198 individuals ready for reproduction from 2000 to 2004 cohorts. The corresponding percentage of known ancestors was estimated as 98.23% for the parent generation, 41.19% for the grandparent generation and 7.00% for the great grandparents generation. The average generation interval for Houbara was computed as 4.64 years. Genetic variability loss per generation was ascertained using the effective population size (), the founder genome equivalent (fge), the effective number of ancestors and founders (fa) and (fe), respectively, for the RP and across each cohort. The results showed no bottleneck events in the breed but some loss of genetic variability just after the initiation of the conservation program. However, the annual effective population size based on the realized increase in inbreeding () was estimated to be 207 for the RP and 1,000 for the WP. With regard to conservation breeding schemes, the genealogical evidence presented here is very useful as it revealed the positive effect of migration on Houbara breeding. The mating strategies will assist in the future control and management of the genetic variability of this population. Zoo Biol. 32:366‐373, 2013. © 2012 Wiley Periodicals, Inc.