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Plants included in the diet of Arabian Sand Gazelle (Reem) from Saudi Arabia
*Address: Environment & Wildlife Consulting, 4 Mokke Str, Windhoek, Namibia. Tel.: +264 61 254550 pckkwrc@yahoo.co.uk (Peter L. Cunningham)
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Received: ,
Accepted: ,
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.
Available online 29 January 2013
Peer review under responsibility of King Saud University.
Abstract
Arabian Sand Gazelles are typical intermediate feeders (browsing and grazing) becoming concentrate selectors during the wet season (grazing) with a preference for short grasses and forbs throughout their range. At least, 80 plant species from 23 families have been published as being utilised by reem, mainly from five protected areas throughout Saudi Arabia. Knowledge of the diet of reem is important in assisting wildlife managers with practical decision making, especially with regard to reintroduction.
Keywords
Gazella subgutturosa marica
Diet
Saudi Arabia
Introduction
The Arabian Sand Gazelle Gazella subgutturosa marica Thomas, 1897 (reem) are classified as “vulnerable” by the IUCN (2008) with 35% of the global population associated with Saudi Arabia (Dunham et al., 2001). Although the species Gazella subgutturosa Guldenstadt 1780 is widespread, occurring from Arabia through the deserts of east and central Asia as far as western China, the subspecies G. s. marica is confined to the Arabian Peninsula (Thouless et al., 1991). Recent evidence indicates that G. s. marica is more closely related to the north-African species Gazella leptoceros and Gazella cuvieri, indicating that G. s. marica and G. s. subgutturosa have evolved independently (Wacher et al., 2010). In addition to Saudi Arabia, reem is found in small numbers in Oman and the coastal and offshore islands along the Arabian Gulf (e.g. United Arab Emirates, Qatar and Bahrain), although the purity of the Gulf populations is questionable making the Saudi Arabian population of international importance (Thouless et al., 1991). Recently, reem numbers have declined dramatically in the wild in Saudi Arabia (Cunningham and Watcher, 2009) yet very little is known about issues as basic as their diet (Habibi 1991, Mohammed and Saleh 1991). For the effective management of herbivore populations, it is crucial to know the diet (Bookhout 1996) especially when introducing reem as has occurred in two protected areas – Mahazat as-Sayd and Uruq Bani M'arid – in Saudi Arabia.
Reem are predominantly viewed as grazers (Thouless et al., 1991) although dwarf shrubs are important browse throughout their range (Harrison and Bates 1991) with Wacher (1995) indicating their use of bulbs, forbs, grasses and occasionally trees (i.e. browse) from Saudi Arabia. Haque (1992) confirms reem being grazers, with grazing preference shown towards Panicum and Stipagrostis grass species in western Saudi Arabia. Plant species utilised by reem in various protected areas in Saudi Arabia have not been well documented with what little is known, published as internal reports and not easily accessible – e.g. Thouless and Al-Bassri (1989) [Al Khunfah]; Robinson et al., (2000) [Harrat al-Harrah]; Haque (1992) [Mahazat as-Sayd]; Wacher (1995) [Uruq Bani M'arid] (See Fig. 1 & Table 1). More recently Cunningham (2009a) confirmed 21 plant species utilised by reem from central Saudi Arabia (Thumamah) indicating the importance of forbs in their diet. This paper attempts to synthesise the plant species known to be included in their diet, from as many unpublished reports as possible, as well as draw some conclusions regarding their diet from Saudi Arabia, in an attempt to assist with future envisaged reintroductions.
Species
Family
Protected Areas
Reference
Arabian Peninsula
Al Khunfah
Harrat al-Harrah
Mahazat as-Sayd
Thumamah
Uruq Bani M'arid
Acacia ehrenbergiana
Fabaceae
*
Robinson (2005)
Acacia ramulosa
Fabaceae
*
Robinson (2005)
Acacia oerfota
Fabaceae
*
Robinson (2005)
Acacia tortilis
Fabaceae
*
*
*
Vesey-Fitzgerald (1952), Asmodé (1990), Haque (1992), Wacher (1995), Robinson (2005), Cunningham (2009b), Ul-Islam et al. (2010), Al-Sodany et al. (2011)
Aerva javanica
Amaranthaceae
*
Robinson (2005)
Anabasis setifera
Chenopodiaceae
*
Thouless and Al-Bassri (1989)
Anastatica hierochuntica
Brassicaceae
*
Thouless and Al-Bassri (1989)
Aristida adscensionis
Poaceae
*
Robinson (2005)
Atriplex leucoclada
Chenopodiaceae
*
Thouless and Tatwany (1989)
Atriplex sp.
Chenopodiaceae
*
Robinson (2005)
Cakile arabica
Brassicaceae
*
Cunningham (2009a)
Calligonum crinitum
Polygonaceae
*
Robinson (1999), Robinson (2005)
Cenchrus ciliaris
Poaceae
*
Robinson (2005)
Centropodia forskalii
Poaceae
*
Robinson (2005)
Centaurea fragilis
Poaceae
*
*
Thouless and Al-Bassri (1989), Robinson (2005)
Centuarea pseudo sinaica
Compositae
*
Cunningham (2009a)
Chenopodium sp.
Chenopodiaceae
*
Robinson (2005)
Chrysopogon plumulosus
Poaceae
*
Robinson (2005)
Citrullus colocynthis
Cucurbitaceae
*
*
Thouless and Al-Bassri (1989), Thouless et al. (1991), Haque (1992)
Convolvulus lineatus
Convolvulaceae
*
Cunningham (2009a)
Convolvulus oxyphyllus
Convolvulaceae
*
Cunningham (2009a)
Convolvulus sp.
Convolvulaceae
*
Wacher (1995)
Cornulaca arabica
Chenopodiaceae
*
Robinson (2005)
Crotalaria aegyptiaca
Fabaceae
*
Wacher (1995), Robinson (1999), Robinson (2005)
Cynodon dactylon
Poaceae
*
Robinson (2005)
Cyperus aucheri
Cyperaceae
*
*
Robinson and Wacher (2001), Robinson (2005)
Dichanthium foveolatum
Poaceae
*
Wacher (1995), Robinson (2005)
Dipcadi unicolor
Hyacinthaceae
*
Wacher (1995)
Dipterygium glaucum
Capparaceae
*
Wacher (1995), Robinson (1999), Strauss et al. (2000), Robinson and Wacher (2001), Robinson (2005)
Ephedra transitoria
Ephedraceae
*
Robinson et al. (2000)
Eremobium aegyptiacum
Brassicaceae
*
Thouless and Al-Bassri (1989)
Euphorbia granulata
Euphorbiaceae
*
*
Thouless and Al-Bassri (1989), Kingdon (1990)
Fagonia bruguieria
Zygophyllaceae
*
Cunningham (2009a)
Fagonia sp.
Zygophyllaceae
*
Haque (1992)
Farsetia burtonia
Cruciferae
*
Robinson (2005)
Farsetia longisiliqua
Cruciferae
*
*
Wacher (1995), Cunningham (2009b)
Farsetia stylosa
Cruciferae
*
Cunningham (2009a)
Farsetia sp.
Cruciferae
*
Wacher (1995)
Haloxylon salicornicum
Chenopodiaceae
*
*
*
Wacher (1995), Robinson et al. (2000), Robinson (2005), Cunningham (2009a)
Heliotropium crispum
Boraginaceae
*
Thouless and Al-Bassri (1989)
Heliotropium digynum
Boraginaceae
*
*
Strauss et al. (2000), Robinson and Wacher (2001), Robinson (2005), Wacher (2005)
Heliotropium ramosissimum
Boraginaceae
*
*
Wacher (1995), Cunningham (2009a)
Indigofera spinosa
Fabaceae
*
*
*
Kingdon (1990), Thouless et al. (1991), Haque (1992), Wacher (1995), Cunningham (2009b)
Kochia indica
Chenopodiaceae
*
Cunningham (2009a)
Lasiurus scindicus
Poaceae
*
*
*
Wacher (1995), Robinson (2005), Cunningham (2009a), Cunningham (2009b), Al-Sodany et al. (2011)
Launaea cassiniana
Compositae
*
Cunningham (2009a)
Limeum arabicum
Aizoaceae
*
Robinson (2005)
Maerua crassifolia
Capparaceae
*
*
Haque (1992), Robinson (2005), Cunningham (2009b)
Moltkiopsis ciliate
Boraginaceae
*
*
Robinson (2005), Cunningham (2009a)
Monsonia nivea
Geraniaceae
*
*
Cunningham (2009a), Cunningham (2009b)
Moretia parviflora
Brassicaceae
*
Cunningham (2009b)
Neurada procumbens
Neuradaceae
*
*
*
*
Thouless and Al-Bassri (1989), Robinson (2005), Cunningham (2009a)
Ochradenus baccatus
Resedaceae
*
Robinson (2005)
Ottochloa compressa
Poaceae
*
Cunningham (2009b), Al-Sodany et al. (2011)
Panicum turgidum
Poaceae
*
*
*
*
Asmodé (1990), Haque (1992), Wacher (1995), Robinson (2005), Cunningham (2009a), Cunningham (2009b), Al-Sodany et al. (2011)
Pennisetum divisum
Poaceae
*
Robinson (2005)
Pituranthos triradiatus
Boraginaceae
*
Thouless and Al-Bassri (1989)
Plantago boissieri
Chenopodiaceae
*
Cunningham (2009a)
Polycarpaea repens
Caryophyllaceae
*
*
Wacher (1995), Cunningham (2009a)
Polygala sp.
Polygalaceae
*
Robinson (2005)
Rhanterium epapposum
Compositae
*
*
*
Vesey-Fitzgerald (1952), Thouless and Al-Bassri (1989), Kingdon (1990), Harrison and Bates (1991), Cunningham (2009a)
Rhynchosia pulverulenta
Fabaceae
*
Robinson (2005)
Rumex vesicarius
Polygonaceae
*
*
Robinson (2005), Cunningham (2009a)
Salsola spinescens
Chenopodiaceae
*
*
Robinson et al. (2000), Cunningham (2009b)
Salsola sp.
Chenopodiaceae
*
*
Thouless and Al-Bassri (1989), Robinson (2005)
Stipagrostis drarii
Poaceae
*
Cunningham (2009a)
Stipagrostis foexiana
Poaceae
*
Wacher (1995)
Stipagrostis obtusa
Poaceae
*
*
Thouless and Al-Bassri (1989), Robinson et al. (2000)
Stipagrostis plumosa
Poaceae
*
Cunningham (2009a), Al-Sodany et al. (2011)
Stipagrostis sp.
Poaceae
*
*
*
*
Thouless and Tatwany (1989), Haque (1992), Robinson (2005), Cunningham (2009b)
Suaeda sp.
Chenopodiaceae
*
Thouless and Al-Bassri (1989), Thouless and Tatwany (1989)
Tephrosia purpurea
Fabaceae
*
Wacher (1995)
Tragus racemosus
Poaceae
*
Robinson (2005)
Tribulus arabicus
Zygophyllaceae
*
Wacher (1995)
Tribulus macropterus
Zygophyllaceae
*
*
Robinson (2005), Cunningham (2009b)
Tribulus pentandrus
Zygophyllaceae
*
Wacher (1995), Robinson (2005)
Tribulus terrestris
Zygophyllaceae
*
Robinson (2005)
Tribulus sp.
Zygophyllaceae
*
*
*
Thouless and Tatwany (1989), Haque (1992)
Trigonella anguina
Fabaceae
*
Thouless and Al-Bassri (1989)
Zygophyllum simplex
Zygophyllaceae
*
Robinson (2005)
Materials and methods
A search on the scientific literature, including unpublished reports – i.e. grey literature – by various authors dating back to 1989, were collected for the Al-Khunfah, Harrat al-Harrah, Mahazat as-Sayd, Thumamah and Uruq Bani Ma'arid protected areas known to have reem populations (Table 1). The various reports mainly include ad hoc data collection of plants included in the diet of reem either conducted during vehicle wildlife census or general habitat assessments following predetermined or random transects covering the entire areas or sections of areas. The different surveyors’ involved and monitoring techniques applied varied between years and were not standardised throughout all the protected areas and thus direct comparisons between years and protected areas cannot be made. Due to the various techniques used and/or applied over the years by various surveyors no attempt has been made here to describe all of these.
Results
Eighty plant species from 23 families have been published as being utilised by reem from five protected areas throughout Saudi Arabia. These consist of Poaceae (17 species), Chenopodaceae (11 species), Fabaceae (9 species), Zygophyllaceae (8 species), Boraginaceae (5 species), Brassicaceae and Cruciferae (4 species each), Compositae and Convolvulaceae (3 species each), Capparaceae and Polygonaceae (2 species each) and one species each for Amaranthaceae, Aizoaceae, Caryophyllaceae, Cucurbitaceae, Cyperaceae, Ephedraceae, Euphorbiaceae, Geraniaceae, Hyacinthaceae, Neuradaceae, Polagalaceae and Resedaceae. Forty-one plant species have been recorded in the diet of reem from Uruq Bani M'arid, 21 from Thumamah, 19 from Harrat al-Harrah, 17 from Al-Khunfah and 14 from Mahazat as-Sayd (Table 1).
Discussion
According to Thouless et al., (1991), reem are predominantly viewed as grazers, feeding on ephemeral plants after rains but generally rely on dry grasses, chenopods and desert melons (i.e. forbs) with a preference shown towards Panicum and Stipagrostis grasses in the Mahazat As-Sayd in Saudi Arabia (Haque, n.d. (1996)), although distinct seasonal changes mostly related to rainfall being apparent. Grasses, especially Stipagrostis species, are utilised widely in Saudi Arabia although forbs (e.g. Convolvulus lanatus, Farsetia stylosa, Heliotropium species, and Neurada procumbens) are preferred (Thouless and Al-Bassri 1989; Wacher 1995; Strauss et al., 2000; Robinson and Wacher 2001; Cunningham 2009a,b). Mohamed and Saleh (1991) confirm the importance of forbs in their diet from Bahrain. During the dry season in western Saudi Arabia, reem survive by foraging mainly on Salsola spinescens shrubs (Cunningham 2009b) and fallen Acacia tortilis pods (Asmodé 1990; Haque 1992; Cunningham 2009b), and occasionally even A. tortilis gum (Cunningham 2009b). Mowlavi (1978) noted that browsing formed the largest part of the diet (86%) of the G. s. subgutturosa – increasing during the drier months – in Iran.
More recent studies conducted by Cunningham (2009b) and Schulz et al., (2012) in Saudi Arabia, indicate that reem are intermediate feeders (browsing and grazing) becoming concentrate selectors during the wet season (grazing) with a preference for short grasses and forbs. These authors indicate that in Mahazat As-Sayd, grasses – including seedlings – that were most heavily utilised, were Octochloa compressa (leaves and occasionally inflorescence) followed by, but not necessarily in order of utilisation, Lasiurus scindicus (leaves), Panicum turgidum (leaves) and Stipagrostis sp. (leaves), although no attempt to quantify grass use was made due to general observation difficulties. Although plant part selection was evident, but not studied, it is known to be important for dorcas gazelle (Gazella dorcas) in Israel (Henley and Ward 2006). The importance of graze for reem in Mahazat as-Sayd was confirmed throughout the year except during autumn – before the rains – when the use of browse dominated. The period of Acacia tortilis leaf drop and height of available foliage would however also affect the use of browse. The movement towards areas that had received rain and an appreciable change in diet from browse to graze during the wet season furthermore indicate the importance of graze. Impala (Stewart 1971; Dunham 1980) and springbok (Antidorcas marsupialis) (Liversidge 1970; Bigalke 1972) from southern Africa and dorcas gazelle from North Africa (Grettenberger 1987) and Israel (Baharav 1982) showed a similar trend when the proportion of grasses in the diet reflected the availability of green grass in the habitat.
Forbs were preferred above grasses – i.e. utilised more – although no attempt was made to quantify this, other than confirming the importance of ‘grazing’ which included grasses and forbs (Cunningham, 2009b). Dietary studies of reem from Bahrain (Mohamed and Saleh 1991) and central Saudi Arabia – Thumamah – (Cunningham, 2009a) also showed a preference for forbs. The importance and selection of forbs above grasses for other herbivores – e.g. tortoises – has also been documented (El Mouden et al., 2006; Hazard et al., 2009).
Dwarf shrubs are also important browse (Harrison and Bates 1991) with Wacher (1995) indicating their occasional use of trees – i.e. browse in southern Saudi Arabia. Mowlavi (1978) noted that browsing formed the largest part of the diet of G. s. subgutturosa especially during the drier months, in Iran. In Mahazat as-Sayd, males utilised A. tortilis and Maerua carssifolia more while females utilised S. spinescens more while browsing (Cunningham, 2009b). According to Gillet and Launay (1990) new flush S. spinescens from Mahazat as-Sayd had a crude protein content of 17.2% and a mineral content of 19% while grasses had lower crude protein contents (e.g. Lasiurus scindicus 12.2% & Panicum turgidum 4.8–6.8%) probably indicating the reason why females selected for S. spinescens. Differences in diet between the sexes for impala and springbok are attributed to their social systems (Van Rooyen and Skinner 1989; Skinner and Smithers 1990) and male springbok physiology being better able to utilise poorer quality fodder (Davies and Skinner 1986) which is probably similar for reem. Crude protein contents for A. tortilis from Sudan indicate lower values between 4.0% and 5.6% although the moisture content is high (48.6–63.7%) making the selection thereof during the dry period's imperative for the survival of dorcas gazelle (Carlisle and Ghorbial 1968; Grettenberger 1987) and dama gazelle (Nanger dama Pallas 1766) in Niger (Ghobrial 1974; Grettenberger and Newby 1986). A. tortilis is also an important source of browse for dorcas gazelle in Israel during summer (Baharav 1980, 1982). Baharav and Rosenzweig (1985) suggest that dorcas gazelle in Israel attempt to optimise water intake during summer rather than energy intake with water content differences between A. tortilis (winter −54%, summer −50%) and grasses (winter – 43%, summer −5%) indicative thereof. Although A. tortilis is not utilised much during summer in Mahazat as-Sayd, as no green leaf flush occurs then, it was replaced by S. spinescens, probably serving the same purpose during this challenging season. Although the plants identified in the diet of reem from Saudi Arabia were not analysed for their nutritional parameters, a nutritional study of desert plants conducted in the United Arab Emirates ranked species with the highest nutritional values (e.g. crude protein, dry matter, ash, ether extract & acid detergent fibre) as Acacia tortilis, Convolvulus sp., Dipterygium glaucum, Farsetia sp., Neurada procumbens, Panicum turgidum and Tribulus sp. (Wensvoort 1992). These species are also preferred by reem from Saudi Arabia (Thouless and Al-Bassri 1989; Wacher 1995; Cunningham, 2009a,b).
The spines of Indigofera spinosa, another shrub utilised occasionally during the extreme dry periods in Mahazat as-Sayd, probably makes it less sought after as indicated by Cooper and Owen-Smith (1986) for other similar spiny browse species. The use and importance of A. tortilis pods, of which an individual tree can produce up to 10 kg (Baharav 1980), was noted for dorcas gazelle in Chad (Newby 1978) and Israel (Baharav 1980). A. tortilis are as important in Mahazat as-Sayd as pods drop during midsummer (August) when very little else is available (Cunningham, 2009b). According to Baharav (1980) ostrich outcompetes dorcas gazelle for pod use in Israel, something that may put additional stress on ostrich and reem during midsummer in Mahazat as-Sayd.
Other, more unconventional, plants included in the diet of reem include seaweeds, along the Caspian and Aral Sea (Kingswood and Blank 1996), leaves of mangrove (Avecennia marina) (Cunningham 2008) and the desert hyacinth (Cistanche tubulosa) (Hornby 2003) in the United Arab Emirates.
Increased knowledge of the diet of reem is expected to assist wildlife managers with determining carrying capacity, assessing viable habitats for future reintroduction programmes, including the overall successful management within protected areas in Saudi Arabia.
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