Wild Gazelles of the Southern Levant: Genetic Profiling Defines New Conservation Priorities

The mountain gazelle (Gazella gazelle), Dorcas gazelle (Gazella Dorcas) and acacia gazelle (Gazella arabica acacia) were historically abundant in the southern Levant, and more specifically in Israel. Anthropogenic and natural changes have caused a rapid decline in gazelle populations, raising concerns about their conservation status and future survival. The genetic profile of 111 wild gazelles from Israel was determined based on three regions of mitochondrial DNA (control region, Cytochrome b and 12S ribosomal RNA) and nine nuclear microsatellite markers. Genetic analysis of the mountain gazelle population, the largest known population of this rare species, revealed adequate diversity levels and gene flow between subpopulations. Nevertheless, ongoing habitat degradation and other human effects, such as poaching, suggest the need for drastic measures to prevent species extinction. Dorcas gazelles in Israel displayed inbreeding within subpopulations while still maintaining considerable genetic diversity overall. This stable population, represented by a distinctive genetic profile, is fragmented and isolated from its relatives in neighboring localities. Based on the genetic profile of a newly sampled subpopulation in Israel, we provide an alternative hypothesis for the historic dispersal of Dorcas gazelle, from the Southern Levant to northern Africa. The small acacia gazelle population was closest to gazelles from the Farasan Islands of Saudi Arabia, based on mitochondrial markers. The two populations did not share haplotypes, suggesting that these two populations may be the last remnant wild gazelles of this species worldwide. Only a dozen acacia gazelles survive in Israel, and urgent steps are needed to ensure the survival of this genetically distinctive lineage. The genetic assessments of our study recognize new conservation priorities for each gazelle species in the Southern Levant.     

Population development of Arabian Gazelles,Gazella arabica,on the Farasan Islands,Saudi Arabia (Mammalia: Bovidae)

The population of the Arabian Gazelle (Gazella arabica) was assessed on Farasan Kebir, the main island of the Farasan Archipelago (Saudi Arabia), from June 2010 to January 2013, using road strip counts. Two methods of estimating the population size were applied to analyse data obtained from the road strip count: (i) the traditional technique after Bothma, with a fixed strip width, and (ii) distance sampling using DISTANCE 6.0. Estimates varied between 483 gazelles (95% CI: 44) in November 2010 and 1070 gazelles (95% CI: 63) in June 2010. The number of gazelles estimated for Farasan Kebir using distance sampling is 2388 gazelles (95% CI: 921) in December 2011, 1199 gazelles (95% CI: 1372) in June 2012, and 1048 gazelles (95% CI:1524) in January 2013. Taking into account previous counts (1988–2009) the population seems, despite considerable variations, surprisingly stable. This may be attributed to a prevailing fishing culture among local residents and thus the absence of traditional hunting as well as the ranger activities on the islands. The disparity between the two estimation methods decreased to only 270 gazelles in January 2013 and provides additional confidence in the future application of both estimation techniques.The traditional technique is recommended as the more practical method for rangers and conservation mangers to determine population changes.     

新疆卡拉麦里山有蹄类自然保护区鹅喉羚遗传多样性及系统发育地位

鹅喉羚是生活于亚欧大陆荒漠、半荒漠地区重要的有蹄类动物。2010年春季,新疆卡拉麦里山有蹄类自然保护区遭遇了60年不遇的雪灾,我们采集了野外救灾发现的130头死亡鹅喉羚肌肉样本,采用PCR和测序技术,研究了鹅喉羚线粒体 DNA 的 Cyt b 基因 1143 bp 核酸序列,发现新疆卡拉麦里山有蹄类自然保护区生存的鹅喉羚单倍型多样性较高(Hd=0.855),核苷酸多样性较低(π=0.00224)。采用邻接法(NJ)、最大似然法(ML)构建单倍型之间的系统发育树,以及network所构建的单倍型间中介网络图都显示出2个遗传分化程度很大的分支,且这2个分支都出现过明显的群体扩张和持续增长。将本研究获得的单倍型H1与Genebank检索获得的瞪羚属其他12个物种Cyt b基因进行了比较,分别采用邻接法(NJ)和最大似然法(ML)构建分子系统树,证明与鹅喉羚最接近的物种为印度瞪羚(Gazella bennettii),鹅喉羚与瞪羚属内物种的分歧时间大约为1.08-2.5百万年(Mya)(Million years ago, Mya)。     

Reproductive strategies in female Mountain and Dorcas gazelles (Gazella gazella gazella and Gazella dorcas)

Observations of reproduction in four gazelle populations in the semi–arid and arid habitats of Israel during three years have revealed intra– and interspecific differences. In the eastern Lower Galilee of northern Israel, female Mountain gazelles (Gazella gazella gazella) reproduce during every month of the year, conceive first at six months of age and exercise long parental care. Females of a population 80 km to the north (Upper Galilee) maintain a seasonal reproductive pattern, conceive first at 18 months of age and have a short parental care period. The latter pattern is similar to the Dorcas gazelle (Gazella dorcas) females of the southern Negev Desert. Interspecific similarities in reproduction of these two populations is attributed to the lack of free water during lactation in both environments where females rely on water available in plant tissue only. The importance of the daily accessibility to water during lactation in female gazelles is discussed. It is suggested that the timing of births and the ability of female gazelles to conceive while lactating are not species-specific characteristics but simply a matter of short-term adaptation to changing environmental conditions common understanding today that animal reproductive strategies are a function of prevailing environmental conditions.     

Genetic diversity and relations of the Goitered gazelle (<Emphasis Type="Italic">Gazella subgutturosa</Emphasis>) groups from Uzbekistan,Turkmenistan, and Azerbaijan: Analysis of the D-loop of mitochondrial DNA

Polymorphism of the nucleotide sequence of a hypervariable fragment of the D-loop (985 bp) of mtDNA in 76 Goitered gazelles of subspecies Gazella subgutturosa subgutturosa from Uzbekistan, Turkmenistan, and Azerbaijan was studied. The genetic similarity of gazelles from Turkmenistan and Uzbekistan has been identified. The population of gazelles from Shirvanskaya steppe reserve (Azerbaijan) is unique and strictly isolated from other groups studied. A high haplotypic (H = 0.9649 ± 0.0091) and relatively low nucleotide diversity (π = 0.0212 ± 0.0105) were noted for all investigated groups of gazelle based on this mtDNA fragment, which is probably related to ecological peculiarities of the species and the history of formation of regional populations.     

Experimental transmission of gastro-intestinal nematodes between sheep (Ovis aries) and Thomson's gazelles (Gazella thomsonii).

Experimental cross-transmission of gastro-intestinal nematodes between Merino sheep (Ovis aries) and Thomson's gazelles (Gazella thomsonii) from similar but separate grazing habitats in Kenya was studied. Cross-transmission did occur with some species but the faecal egg counts of sheep were higher than the gazelles' following infection with larvae isolated from either sheep or gazelles. Of the 11 gastro-intestinal nematodes which became established in gazelles following infection with larvae cultured from nematodes in gazelles, only Haemonchus contortus, Trichostrongylus probolurus and Cooperia hungi were infective for sheep. Following infection with larvae of either sheep or gazelle origin, the H. contortus recovered from the sheep at necropsy were more numerous and had greater average weights, lengths and spicule lengths than those recovered from the gazelles. This would suggest that H. contortus is primarily a sheep parasite. It is concluded that Thomson's gazelles probably would not contribute significantly to the problem of haemonchosis in sheep in areas of shared grazing, unless efforts were being made to eradicate the parasite from sheep, in which case the gazelles would act as a continuing reservoir of infection.     

Coagulation profile and platelet parameters of the Arabian sand gazelle (Gazella subgutturosa marica): comparison with humans and camels

During March 2009, we evaluated the hemostatic profile and platelet indices of 18 Arabian sand gazelles (Gazella subgutturosa marica) and compared the results with those from humans and camels (Camelus dromedarius). Gazelles and camels had shorter activated partial thromboplastin times, lower proconvertin and higher antihemophilic factor coagulation activity, and plasma fibrinogen levels than humans. Prothrombin time was longer in sand gazelles and shorter in camels than it was in humans. Plasma thromboplastin component, Stuart factor, and plasma thromboplastin antecedent were similar in gazelles, humans, and camels, whereas the platelet count of the sand gazelle was significantly higher than it was for camels and humans.     

Fecal progesterone metabolites and ovarian activity in cycling and pregnant mountain gazelles (Gazella gazella)

Fecal reproductive progestagen monitoring in the mountain gazelle (Gazella gazella) provided a non-invasive method for tracking reproductive cycling, estimating age of sexual maturity and diagnosing pregnancy in this species of gazelle. Fresh fecal samples were collected from eight female mountain gazelle (Gazella gazella) for a period of two months. Two of the animals were pregnant while the other six were not. Using the progestagen profile the luteal phase, interluteal (follicular) phase and estrous cycle in adult female gazelles were determined to be 12.5 ± 1.2, 5.9 ± 0.59 and 18.8 ± 0.98 days respectively. Significant inter-animal differences in fecal progestagen concentration were observed in both the luteal and follicular phases. Significant differences were observed in the levels of fecal progestagen between cycling females and females in late pregnancy. Low concentrations of fecal progestagen in females aged less than 18 months old indicated that sexual maturity in captivity is not attained before that age.     

Post-mortem semen cryopreservation and characterization in two different endangered gazelle species (Gazella gazella and Gazella dorcas) and one subspecies (Gazella gazelle acaiae)

Both Gazella gazella and Gazella dorcas are endangered species with continually dwindling population size, yet basic knowledge on their spermatozoa is missing. Semen collected post-mortem (PM) from the cauda epididymis of five adult gazelles (three Gazella gazella gazella, one Gazella gazella acaiae and one G. dorcas) was cryopreserved using directional freezing of large volumes (8 mL) with egg-yolk-free extender. Sperm size measurements and SYBR-14/propodium iodide (PI) viability stain validation for use in gazelles were conducted. Post-thaw characterization included motility, viability, acrosome damage evaluation, computerized motility characterization and morphology and sperm motility index (SMI) was calculated. Extracted sperm motility was 71.67+/-11.67% (mean+/-S.E.M.). Post-thaw motility ranged between 15% and 63%, viability was 57.49+/-3.24%, intact acrosome was detected in 63.74+/-2.6% (median 64.8%, upper/lower quartiles 71.79%, 61.82%), and normal morphology ranged between 41% and 63%. Motility characterization showed two sub-groups-highly active and progressively motile spermatozoa with SMI of 62.75+/-0.38 and low activity and poorly progressive with SMI of 46.16+/-1.53. Our results indicate that PM preservation of gazelle spermatozoa with satisfactory post-thaw viability is possible and cryobanking is achievable.     

Food preferences and tooth wear in the sand gazelle (Gazella marica)

Food preferences of the sand gazelle (Gazella marica) from the Mahazat as-Sayd Protected Area in Saudi Arabia were evaluated using focal animal sampling in conjunction with an eco-morphological method examining two parameters of tooth wear, i.e., occlusal relief and cusp shape. Observations of live, free-ranging animals (n = 53) showed that sand gazelles generally consumed more grass (58.4%) than browse (41.6%). However, during the dry season, gazelles spent significantly more time browsing (51.0%) and less time grazing (49.0%) than under wet conditions (browsing: 17.6%; grazing: 82.4%). Thus, consistent with predictions, sand gazelles are intermediate feeders but shift towards browsing when grass is scarce. The mesowear signature of the sand gazelle is consistent with a grazing signal in other ruminants. In other words, the browse component of the diets of live animals was not reflected in the tooth wear. This could have occurred because browse is less abrasive than grass, but more likely because all food types are heavily abrasive in this dusty habitat. We conclude that the sand gazelle population in Mahazat as-Sayd encounters a highly abrasive diet, which has implications for their ability to meet nutritional demands.     

Utility of island populations in re‐introduction programmes – relationships between Arabian gazelles (Gazella arabica) from the Farasan Archipelago and endangered mainland populations

Understanding local adaptation and population differentiation is vital to the success of re‐introduction initiatives. As other mammals living on islands, Arabian gazelles (G. arabica) show reduced body size on the Farasan archipelago, which we corroborated in this study through morphometric analyses of skulls. In the light of the steep population decline on the Arabian Peninsula – but stable population development on the archipelago – we tested the potential suitability of Farasan gazelles as a source for re‐introductions on the mainland. We therefore investigated genetic differentiation between Farasan and mainland populations using eleven nuclear microsatellite loci and detected a distinct genetic cluster exclusively present on the archipelago, which we inferred to be separated from the mainland cluster for less than 2000 years. About 30% of sampled individuals from Farasan Islands showed assignment to a mainland cluster with signs of ongoing introgression. Analyses using the isolation‐with‐migration model confirmed recent (probably human‐induced) bidirectional exchange of gazelles between mainland and island populations. Hence, the surprisingly uniform island dwarfism most likely reflects phenotypic plasticity, that is, altered morphology as a direct consequence of harsh environmental conditions and resource limitation on the archipelago. Should a further decline of Arabian gazelles on the mainland necessitate restocking in the future, Farasan gazelles may thus become an additional source for captive breeding programmes.     

Utilization of harvester ant nest sites by Persian goitered gazelle in steppes of central Iran

Ants are among the most important elements in many ecosystems and known as famous ecosystem engineers. By changing physical and chemical properties of soil, ants may provide suitable habitats for other species. Based on previous observations, we hypothesized that Persian goitered gazelles (Gazella subgutturosa subgutturosa) exhibit a preference for utilizing sites close to seed harvester ant (Messor spp.) nests. We tested our hypothesis by (1) mapping the occurrence of harvester ant nests and aggregated gazelle pellet groups along 31 strip transects, (2) monitoring pellet group accumulation bimonthly at 56 pairs of permanent plots established on ant nests and at adjacent control sites for a complete year, and (3) comparing vegetation and soil parameters between ant nest sites used by gazelles and paired control plots without ant nests. Although the area of Messor spp. nest sites covered only about 0.29% of the sampled transects, 84% of the gazelle pellet group aggregation sites were positioned upon ant nests, suggesting that gazelles actively selected Messor spp. nest sites. Pair-wise comparisons between ant nest plots and paired control plots also confirmed higher use of ant nest sites by gazelles compared to sites without ant nests in all time periods. Percent soil organic matter, percent cover of gravel, and annual herb vegetation significantly differed between ant nest and paired control plots in all the vegetation communities. We suggest that the alterations brought about by harvester ants on soil and vegetation make these sites attractive to gazelles. Gazelle territoriality behaviour and use of ant nests as bedding sites may be the reasons for selection of ant nest sites by gazelles.     

Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles

We examined the effects of herbivory by the dorcas gazelle, Gazella dorcas, on different phenological stages of the lily Pancratium sickenbergeri from 1990–1996 in the Negev desert, Israel. We placed particular emphasis on the role of gazelle herbivory on selecting for plant defences and the effectiveness of these defences against subsequent herbivory. In the summer months, the gazelles dig in the sand to remove all or part of the bulb of the lily. Plants with partially-consumed bulbs were less likely to produce leaves the following winter and probably have lower lifetime flower production. Herbivory has resulted in greater downward growth of the bulb in populations with herbivory than those without herbivory, which reduces the probability that the entire plant will be consumed. Gazelles eat the leaves in the winter; this herbivory has a negative impact on leaf growth rates. However, the production of calcium oxalate limits gazelle consumption to the tips, and consequently reduces the effects of leaf herbivory. In the fall, the gazelles consumed virtually all flowers, yet we found no defence or growth strategy that might ameliorate this impact, with the possible exception of forgoing the output of a second flower stalk after the first has been consumed. The results of this study suggest that lilies employ different strategies to resist gazelle herbivory, and that these strategies are dependent on the phenological stage that is eaten. Avoidance by defence is the strategy in the leaves, avoidance by escape is utilized in bulbs. Forgoing the output of a second flower stalk after the first has been consumed can be considered as a form of escape based on a bet-hedging strategy or a shift in energy allocation.     

Characterization of the spatial distribution of latrines in reintroduced mountain gazelles: do latrines demarcate female group home ranges?

Mountain gazelle Gazella gazella in Saudi Arabia are listed as 'vulnerable' by the IUCN. At present, the species' survival is secured by extensive captive-breeding programmes and reintroductions into protected areas. Two reintroduction attempts (Ibex Reserve and Uruq Bani Ma'Arid protected areas) in Saudi Arabia have been undertaken in the past two decades. Post-monitoring of released individuals is essential for the success of such reintroduction programmes; however, cryptic species like mountain gazelles are extremely difficult to observe directly. As radio-tracking is a cost-intensive and invasive post-monitoring technique, we asked: how can reintroduced or remnant pockets of natural gazelle populations be monitored indirectly ? Here, we propose the use of latrine mapping as an effective, cost-efficient and non-invasive tool to survey the social organization of reintroduced mountain gazelles as an indicator for repatriation success. In this study, we used released radio-collared animals to characterize the spatial distribution of latrines within female group home ranges. Distance to the next latrine, latrine size, as well as numbers of fresh faecal pellet groups per latrine or presence of urination marks were used as dependent variables for step-wise backward multiple regressions and were correlated with various ecological factors. Most dependent variables were correlated with distance or direction from the nearest tree, but not indicative of home-range cores. Only latrine densities were distinctly higher in core areas of female group home ranges, and no pattern of peripheral marking was detected. Hence, latrine density is a good indicator of home-range use in female group home ranges. Mapping latrines and determining latrine densities are therefore the methods of choice to survey mountain gazelle populations.     

Factors affecting the distribution of dorcas gazelle

The dorcas gazelle Gazella dorcas was very common and widespread in Tunisia. Nowadays, only some small isolated populations still survive in the desert areas of the southern part of the country. Factors affecting the distribution of this species in Tunisia have never been investigated despite the importance of such investigations for elaborating long-term conservation plans for the remaining wild populations. Using data on gazelle occurrence and on a set of habitat and human variables collected in south-eastern Tunisia, we aimed to identify the factors affecting gazelle distribution in this area. In particular, we investigated the relevance of habitat versus human factors for gazelle occurrence probability. As predicted, we found that human variables were the most relevant factors shaping the distribution patterns of gazelles in the studied area. Gazelles tended to avoid areas where agricultural development has occurred but did not seem to be disturbed by livestock. Overall, our results suggest that the occurrence probability of dorcas gazelle in southern Tunisia was mainly dependent on human presence and land use, rather than habitat characteristics. The recent intensification of agriculture in the more remote areas of southern Tunisia may thus constitute a serious threat to the conservation of this endangered species.     

A multivariate statistical study of skull measurements of five taxa of gazelles

A multivariate analysis using canonical variates and the D² test show that five taxa of Palaearctic gazelles examined are distinct. Several forms of gazelles of dubious taxonomic position were also compared on the canonical axes, with conclusions not dissimilar to those of recent workers on the Arabian gazelles, viz. that there are three distinct species in the Arabian peninsula; Gazella dorcas saudiya, Gazella gazella arabica and Gazella subgutturosa marica. Gazella dorcas populations in Somalia have a local form in G. dorcas pelzelni distinct in horns but not in skull measurements from Gazella spekei in the nearby highlands.     

道路交通对鹅喉羚昼间集群特征和警戒行为的影响

分析道路交通对濒危有蹄类动物行为模式的影响,阐明其行为反馈与适应机制,对制定道路工程干扰下濒危物种的保护方案具有重要意义。2015年和2016年6-8月,调查了国道216线白昼运营对新疆卡拉麦里山有蹄类野生动物自然保护区鹅喉羚(Gazella subgutturosa)集群特征和警戒行为的影响。研究发现,国道216线的扰动导致鹅喉羚集群规模显著增加;随着距国道216线距离越近,鹅喉羚警戒行为投入时间越多,距离道路500m可能是国道216线对鹅喉羚集群和警戒行为影响的阈值。本研究结果表明,道路带来的人为干扰与捕食风险相似,迫使鹅喉羚调节其集群规模和警戒水平。未来应加强道路等交通工程影响下保护区内野生动物的行为反馈和适应机制研究,据此提出减缓措施,降低道路对野生动物的负面影响。     

The postnatal ontogeny of the sexually dimorphic vocal apparatus in goitred gazelles (Gazella subgutturosa)

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male‐specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age‐classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade‐off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826–844, 2016. © 2016 Wiley Periodicals, Inc.     

原羚属分类地位研究兼论中国羚羊的分类

中国羚羊类动物在世界羚羊类动物中有着特殊的地位,其中普氏原羚、藏原羚和藏羚是中国特有的珍稀物种,普氏原羚是极度濒危动物.开展中国羚羊类动物的分类和进化研究是当务之急.本研究利用形态特征、头骨测量及线粒体DNA的12S rRNA(440 bp)和16S rRNA(590 bp)对原羚属的分类地位及中国其他几种羚羊分类地位进行了探讨,发现对质量性状和数量性状数据的聚类分析的结果差异大,而且质量性状的聚类结果比较符合传统的分类系统.分子分类也得到相似结果,但在属下的分析存在较大差异.7种牛科动物的12S rRNA和16S rRNA序列差异分别为0.2%～7.1%和0.3%～8.4%.系统进化分析表明原羚属3种羚羊形成单系群,且蒙古瞪羚与普氏原羚的关系较藏原羚与普氏原羚的关系近.赛加羚应归宿于羚羊亚科,而不是与羊亚科的藏羚形成独立的赛加羚亚科.原羚属的进化可能与青藏高原的隆起有关.