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VOL 27 NO 4 OCTOBER 1993 Bilkis in - status and taxonomic relationships

Arnaud Greth, Douglas Williamson, Colin Groves, Georg Schwede and Marc Vassart

Bilkis gazelle Gazella bilkis was first described in 1985 from material collected in Yemen in 1951. No new information about the has been forthcoming since then and the 's current status is uncertain in two respects. First, it is difficult to establish the taxonomic relationship between G. bilkis and a possible subspecies of the , G. gazella erlangeri, which also occurs in the south-west Arabian peninsula. Secondly, uncontrolled hunting and the general lack of conservation measures in Yemen mean that, if it does still survive, its continued existence is far from assured. Systematic field surveys and taxonomic research are urgently needed to clarify the status of this animal and draw up conservation measures.

Introduction 1991) but at least three other subspecies of G. gazella as well as Bilkis gazelle are still in jeop- Given the rate at which tropical forests are ardy. Because information on all the being destroyed, it is relatively easy to under- is either very scarce or non-existent, it is very stand how cryptic rain-forest invertebrates difficult to plan conservation measures. with miniscule ranges can become extinct Priority should, therefore, be given to taxo- without being known to science, but it is star- nomic studies and field surveys in order to tling to realize that a similar fate could befall formulate and initiate a conservation strategy, the Bilkis gazelle Gazella bilkis, a medium- as well as immediate remedial action. sized antelope in the Arabian peninsula. This paper presents all available infor- Bilkis gazelle was described by Groves and mation on Bilkis gazelle and emphasizes the Lay (1985) from museum specimens collected urgency of undertaking field surveys and tax- in Yemen in 1951 and named in honour of the onomic research to clarify its status and facili- Queen of Sheba. No further material or infor- tate its conservation. mation has been forthcoming since 1951 and there is none known in captivity. To compre- hend fully the problems regarding G. bilkis, an Gazella bilkis and the dark forms of G. overview of other gazelle taxa in the Arabian gazella in the southern Arabian peninsula is necessary. The taxonomic issue is peninsula confused by the presence of another poorly understood gazelle in the same region G. gazella erlangeri, which is believed to be a sub- species of the mountain gazelle. The taxonomy of the genus Gazella is con- In 1987, Ryder emphasized the 'urgent need sidered to be one of the most equivocal among for conservation action' for some gazelle groups (Groves and Harrison, 1967). species. The situation has recently improved The classification was modified recently, in the north of the Arabian peninsula for the changing the status of some taxa from sub- sand gazelle G. subgutturosa marica and the species to species (Groves, 1969; Furley et al, mountain gazelle G. g. gazella (Thouless et al., 1988), but taxonomic relationships between 239

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and within a number of species are still un- the paler coat, as well as by many skull char- clear. acteristics (Groves and Lay, 1985). A second Groves and Lay (1985) described G. bilkis subspecies, G. g. farasani (Thouless and Al from five specimens (skins and skulls) de- Bassri, 1991), is restricted to the coral archipel- posited in the Field Museum of Natural ago of Farasan, 30 km north of the Yemen bor- History in Chicago by H. Hoogstraal in 1951, der in the Red Sea (Figure 1). A third, G. g. and one skull presented to the Natural History muscatensis, with a pronounced dark grey coat Museum, London, by W. T. Blanford in 1869. (Groves, 1989), is restricted to the coastal strip According to these authors, a number of fea- of northern Oman (Figure 1). tures of the skull, including the shape of the The fourth subspecies, G. g. erlangeri horns (straight with 12-15 rings in the male, (Groves et al., in prep.), is more controversial long with clearly developed rings in the fe- from a taxonomic point of view and its differ- male), and the morphology of teeth, nasal and entiation from G. bilkis is still unclear. It can be premaxillary bones clearly differentiated bilkis distinguished from G. g. com by its small size from other species of gazelles. The colour pat- and dark colour. Described by Neumann terns were also distinct: the body was very (1906) as G. arabica erlangeri from Lahej, north dark with paler fur on the flanks, haunches of Aden, based on a coloured plate (pi. 59) in and legs, there was a very thick flank stripe, Sclater and Thomas (1898), and recently resur- black and conspicuous in the field, and a rected as G. g. erlangeri (Groves et al., in prep.), white line on the inside of the thigh continu- this taxon is possibly sympatric with G. bilkis; ing down the shank. As a diagnostic feature, two specimens from Ma'bar, Yemen (14°46' N, the bilkis gazelle is the darkest species of the 44°21'E), in the Field Museum of Natural genus. History, Chicago, recorded by Groves and Lay At least three other species of gazelles, G. (1985) as G. g. cora, are more likely to be G. g. subgutturosa, G. saudiya and G. gazella (Groves erlangeri. Although Groves and Lay (1985) and Harrison, 1967) were widely distributed proposed that these two taxa are not conspe- throughout the Arabian peninsula. They will cific because of probable sympatry and differ- be discussed here briefly to make a clear dis- ent morphological patterns, scientific evidence tinction between the two taxa with which we is still too weak to classify them as two dis- are mainly concerned. The Arabian sand tinct taxa. Cytogenetics and molecular tech- gazelle G. subgutturosa marica cannot be mis- niques are necessary to clarify the picture. taken for any other species, being very pale in Chromosome studies of G. g. cora and G. g. colour and living in sandy areas (Groves, erlangeri have shown that both subspecies 1989). The so-called 'Arabian dorcas' gazelle have 34 chromosomes in females and 35 in G. saudiya, probably either on the verge of ex- males. These numbers are identical to the ones tinction or already , is small found in G. g. gazella (Wahrman et al., 1973), and sandy-brown in colour with long, straight confirming that these two taxa should be con- horns in both sexes (Groves, 1989). sidered as subspecies of G. gazella. Blood en- Increasingly, it has been suggested that this zyme studies on G. g. gazella, G. g. cora, G. g. gazelle is a distinct species, unrelated to erlangeri and G. g. farasani also showed that African dorcas gazelles (Groves, 1989); recent these taxa are closely related (Vassart et al., in cytogenetic studies strongly corroborate this press). (Rebholz et a\., 1991), but it is still under inves- G. gazella has a large phenotypic variability tigation. and some subspecies in Israel and Iran have The situation of the mountain gazelle G. not yet been described (Karami and Groves, gazella is more complicated, because four sub- 1992; Mendelssohn et al., in press). Special at- species occur in the south of the Arabian tention should be paid to the taxnomy of this peninsula (Figure 1). One, G. g. cora, which is species to allow a clear distinction of taxo- reported to be sympatric with G. bilkis nomic units and to adopt the appropriate con- (Groves, 1989), can be distinguished from it by servation measures.

240 ORYX VOL 27 NO 4 OCTOBER 1993

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Biological information There is almost no information available on the biology and distribution of G. bilkis. All the specimens collected in 1951 came from the mountainous area of Ta'izz (13°35'N,44° 02'E), 200 km south of Saana (Figure 1). Localities in- clude El Hauban in Wadi Maleh, Usaifira and Jabal Zarba (Groves and Lay, 1985; Harrison and Bates, 1991). They were either solitary or in small groups on euphorbia-covered slopes, which were separated from cultivated areas by hills (Sanborn and Hoogstraal, 1953). No other biological data or photographs have been published. A limited survey was carried out in February 1992 by A.G. in the mountains (Jebbel Sabir, Jebbel Samah) between Ta'izz and Al Thurbah, 50 kms to the south. Neither gazelles nor signs of their presence were found. Photographs of gazelles were shown to Gazella gazella erhngeri male kept at the NWRC (S. at least 100 local people in all the villages Saustier/NWRC). visited. All replied that gazelles had not been seen in the area for several decades. No known captive population of G. bilkis ex- It has been suggested that G. bilkis is en- ists in the world. Chester and Marwell zoos in demic to Yemen (Groves and Lay, 1985), but UK maintain small groups of gazelles, which no systematic field survey of its range has ever may include some individuals descended been conducted, and, considering the biogeog- from G. g. cora and G. g. erlangeri hybridized raphy of the Asir mountain range and the re- with G. bilkis. A small group (identified from gional distribution of other species, such as G. photographs by C. G.) was kept in Qatar in g. cora, it is possible that it occurred or even Sheik Al-Thani's collection (Al Wabra, near still exists in , at least in the south Shahaniyah) but they all died without issue. (Groves, 1989).

SAUDI ARABIA \ Muscat

< Riyadh V ~~ \^0MAN N S^-Taif

Najran y—' "*\ /Saana

V Fa rasan Islands ^\^* w*

Ta'izz " Aden H G. gazella cora a G gaze/la erlangeri Figure 1. Presumed range of the G. gazella muscalensis different subspecies of G. gazella 400 km m (• : G. g. famsani) and of G. bilkis

ORYX VOL 27 NO 4 OCTOBER 1993 241

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There is almost no information available for were exchanged with private collections and G. g. erlangeri. According to local bedouins, added to the KKWRC herd during 1992. two forms of gazelles occur in the Asir moun- tains in south-west of Saudi Arabia and the nearby coastal plain, the Tihama (M. Shobrak, Conservation status pers. comm.). One, called 'idmi' is light brown in colour and is almost certainly G. g. com. The The rich biological diversity and high level of other one, smaller and darker, is probably G. endemism in the south-west Arabian penin- g. erlangeri (Groves et ah, in prep.). There have sula contrasts with the lack of information on been no recent sightings of this form. its natural history and conservation impor- Specimens in the Natural History Museum, tance. A few ornithological expeditions have London, and in the Field Museum of Natural visited North Yemen since 1965 (Cornwallis History, Chicago, have been collected near and Porter, 1982) but none reported sightings Aden or Ta'izz (Yemen) and near Taif (Saudi of Bilkis gazelles and R. F. Porter (pers. Arabia). One farmer reported that in 1992 he comm.) saw no gazelles at all during six expe- regularly hunted small gazelles 'the colour of ditions in North Yemen between 1979 and volcanic stones' near Lahej. This information 1987. corresponds with Neumann's (1906) descrip- The complete failure to locate Bilkis gazelles tion of gazelles caught in the same area. in the wild and the absence of conservation Animal dealers from Saudi Arabia or measures in Yemen indicate that if it survives bedouins say that these gazelles are still often at all its situation is desperate (unless G. bilkis caught in Yemen, in the area between Najran and G. g. erlangeri are proved to be conspe- and Sa'dah, near the border of Yemen and cific). Automatic rifles are widely available in Saudi Arabia (Figure 1). Yemen and wildlife is generally over-hunted. While no captive population exists of G. g. During the visit of A. G. to Yemen in February erlangeri outside the Middle East, this gazelle 1992, some Yemeni people reported that rela- can still be found in reasonable numbers in tives or farmers still regularly hunted gazelles captivity, particularly in Saudi Arabia. Their in some places, such as the Lahej region and docile disposition makes them popular as pets the Saham wadi, near Hoddeida. Moreover, and G. g. erlangeri is one of the most common the recent economic development of reunified gazelle species in the numerous private collec- Yemen following the discovery of oil is inten- tions in the Kingdom. The illegal trade in sifying habitat degradation and causing a de- these , which probably come from cline in wildlife. Yemen or from southern Saudi Arabia, indi- cates that this subspecies still occurs some- where in good numbers in the wild. In 1991, a Questionnaire about dark forms of herd of 25 gazelles was found in a pet shop in gazelles in Yemen Jeddah, called 'Beautiful Creatures'. According to the owner, the animals came To clarify the taxonomic relationships be- from a location near Aden. Since then, other tween G. bilkis and G. g. erlangeri and to collect groups have been seen regularly in this shop. biological information on these two taxa, a In 1987 a small captive herd was created at the questionnaire and a set of colour prints of the National Wildlife Research Center (NWRC) G. g. erlangeri herd kept at the NWRC were with three individuals (one male, two females) sent to 25 people (10 antelope specialists, three given by the Emir of Najran. They are re- Yemeni wildlife professionals, four people ported to be from an area in Yemen, close to from the zoo community, three people in the Saudi border. The herd was transferred to charge of conservation organizations in the the King Khalid Wildlife Research Center Middle East and five others, including or- (KKWRC) near Riyadh in January 1992. nithologists, involved in surveys in Yemen). A Nineteen individuals (11 males, eight females) note was also published in the Bulletin of the

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Two male Arabian sand gazelles (Gazella siibgutturosa market) fight- ing (A. Vareille/NWRC).

Ornithological Society of the Middle East (Greth, with the University of California, La Jolla, San 1991) and in Gnusletter, which is published by Diego, as well as other institutions. The main the IUCN/SSC Antelope Specialist Group. aim of this study is to clarify the taxonomic Of the 15 responses obtained 10 said they status of G. bilkis and G. g. erlangeri (and other had no information. Of the five positive re- taxa), by comparing DNA sequences in the sponses, two experts identified the gazelles on hair of living specimens with the type speci- the prints as G. g. ssp., one as G. g. gazella, one mens. If it is possible to extract DNA from the as G. bilkis (for some of the pictures) and one hairs of museum specimens several decades as a mixed herd of G. gazella and G. bilkis. The old, this study might help to determine rela- phenotypic appearance of the NWRC herd is tions between G. g. erlangeri and G. bilkis. quite homogeneous. Even though the photo- graphs sent for the inquiry were perhaps not of ideal quality for taxonomic identification, Conservation action the contradictory answers obtained emphasize the taxonomic problems. International conservation funds are needed urgently for a preliminary survey in Yemen. If G. bilkis or/and G. g. erlangeri is/are dis- Proposals and recommendations covered, an ecological study should be con- ducted to define its/their distribution, habitat requirements, population status and the major Taxonomic research threats. For both taxa, these studies should be A joint effort should be made by geneticists, concluded with a population and habitat via- scientists involved in gazelle taxonomy, field bility analysis. It is also important to recall researchers and zoo managers to apply mod- that the situation of G. g. cora is precarious in ern genetic techniques on all available samples the Asir mountains and the coastal plains of of the taxa discussed here. Allozyme and cyto- the Tihama in Saudi Arabia (Thouless et ah, genetic studies should provide valuable infor- 1991). Appropriate conservation measures mation. The best method may be the compari- should be urgently taken by implementing son of mitochondrial DNA, because the protected areas and enforcing hunting laws. differentiation of the genome of the taxa con- Although in situ conservation must remain cerned is probably relatively recent. This the priority, the implementation of a captive- study should of course include G. bilkis and breeding programme in co-operation with the the different subspecies of G. gazella, with par- international zoo community and the con- ticular attention being given to G. g. erlangeri cerned specialist groups (SSC/IUCN) should and G. g. muscatensis. be considered for all relevant taxa. Individuals As a step towards this, Saudi Arabia's of non-viable populations could be captured National Commission for Wildlife Conservation to serve as founder stock. and Development (NCWCD) has initiated an All these activities should lead to the formu- innovative research project in collaboration lation of an integrated conservation action ORYX VOL 27 NO 4 OCTOBER 1993 243

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plan for the different gazelle taxa within 2 Groves, C.P. and Lay, D.M. 1985. A new species of years, based on collaboration between re- the genus Gazella (MammaliaArtiodactyla: gional governments and different inter- ) from the Arabian peninsula. Mammalia, national conservation institutions. 49, 27-36. Groves, C.P., Thouless, C. and Vassart, M. In press. Assuming that Bilis gazelle still survives, its Subspecies of Gazella gazella in Saudi Arabia. situation must be very precarious. To avoid a Fauna of Saudi Arabia. re-run of Operation Oryx, which in 1962 saved Karami, M. and Groves, C.P. 1992. A mammal the last Arabian oryx by drastic and expensive species new for Iran: Gazella gazella Pallas, 1766 measures, urgent steps need to be taken to (Artiodactyla, Bovidae). In Proceedings 'Ungulates study the dark forms of gazelle in Yemen and '91' (eds F. Spitz, G. Janeau, G. Gonzalez and S. Saudi Arabia to provide a basis for planning Aulagnier), pp. 361-364. SFEPM, Paris. Mendelssohn, H., Yom-Tov, Y. and Groves, C.P. In their conservation. press. Gazella gazella. Mammalian Species. Neumann, O. 1906. Ueber einige Gazellen und Kuh- Antilopen. S. ber. Ges. naturf. Freunde Berlin, 237- Acknowledgmen ts 247. The authors acknowledge with great respect and ap- Rebholz, W.E.R., Williamson, D. and Rietkerk, F. preciation the work done by all the staff of the 1991. Saudi gazelle (Gazella saudiya) is not a sub- NCWCD for the conservation of gazelle species in species of . Zoo Biol. 10,485^489. the Arabian peninsula, and particularly HRH Prince Ryder, O.A. 1987. Conservation action for gazelles: Saud Al Faisal, who initiated all these efforts, and An urgent need. Trends Ecol. Evol. 2,143-144. Professor A. Abuzinada, Secretary-General of the Sanborn, C.C. and Hoogstraal, H. 1953. Some mam- NCWCD. T. Abaigar, R. H. Daly, R. Estes, J. mals of Yemen and their ectoparasites. Fieldiana, Kingdon, C. Magin, H. Mendelssohn, J. Newby and Zool. 34, 229-252. R. Porter helped us to gather information about the Thouless, C.R. and Al Bassri, K. 1991. Taxonomic Bilkis gazelle. J. F. Asmode, J. Dolan, J. Grainger, L. status of the Farasan Island gazelle. /. Zool. Lond, Granjon, A. R. Khoja, N. Lindsay, F. Rietkerk, M. 223,151-159. Shobrak gave useful information or comments on Thouless, C.R., Grainger, J.G., Shobrak, M. and the early draft and helped finalize the proposals. Habibi, K. 1991. Conservation status of gazelles in Saudi Arabia. Biol. Conserv. 58, 85-98. Vassart, M., Granjon, L., Greth, A. and Catzeflis, References F.M. 1993. Genetic relationships of endangered Gazella species from the Arabian peninsula: an Cornwallis, L. and Porter, R.F. 1982. Spring obser- isozyme survey. Can. f. Zool., in press. vations on the birds of North Yemen. Sandgrouse, Wahrman, J., Richler, C, Goitein, R., Horowitz, A. 4,1-36. and Mendelssohn H. Multiple sex chromosome Furley, C.W., Tichy, H. and Uerpmann, H.P. 1988. evolution, hybridization, and differential X chro- Systematic and chromosomes of the Indian mosome inactivation in gazelles. In Jerusalem gazelle, Gazella bennetti (Sykes, 1831). Z. Chromosome Conference, abstracts of additional pa- Saugetierk, 53, 48-54. pers and demonstrations. Chromosomes Today, 42, Harrison, D.L. and Bates, P.J.J. 1991. The of 434-435. Arabia. Harrison Zoological Museum Publications, Sevenoaks, England. Arnaud Greth, 3 rue Larochelle, 75014 Paris, France. Greth, A. 1991. Gazelles in Yemen and Southern Georg Schwede and Marc Vassart, National Wildlife Saudi Arabia. Bulletin of the Ornithological Society Research Center (National Commission for Wildlife of the Middle East, 27, Autumn, 39. Conservation and Development), PO Box 1086, Taif, Groves, C.P. 1969. On the smaller gazelles of the Saudi Arabia. genus Gazella de Blainville, 1816. Z. Saugetierk, 34, Douglas Williamson, King Khalid Wildlife Research 38-60. Center (National Commission for Wildlife Groves, C.P. 1989. The gazelles of the Arabian Conservation and Development), PO Box 61681, peninsula. In Wildlife Conservation and Development Riyadh 11575, Saudi Arabia. in Saudi Arabia. Proceedings of First Symposium (edsColin Groves, The Australian National University, A. H. Abuzinada, P. D. Goriup and I. A. Nader), Department of Prehistory and Anthropology, GPO pp. 237-248. NCWCD, Riyadh, Saudi Arabia. Box 4, Canberra, ACT 2601, Australia. Groves, C.P. and Harrison, D.L. 1967. The taxonomy of the gazelles (genus Gazella) of Arabia. /. Zool., Lond. 152, 381-387. 244 ORYX VOL 27 NO 4 OCTOBER 1993

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