Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region

Small Ruminant Research 91 (2010) 3–12

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Review

Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region夽 Hassan M. El Shaer ∗ Animal Nutrition Department, Desert Research Center, 1 Matahaf El Mataria St., P.O. Box 11753, Mataria, Cairo, Egypt

a r t i c l e

i n f o

Article history: Available online 6 March 2010 Keywords: Halophytes Salt-tolerant plants Livestock Feeds Biomass Production Nutritive value Arid and semi-arid regions

a b s t r a c t This review paper updates knowledge on the fodder potential of a wide range of halophytes and salt-tolerant forages. These plants can produce relatively high consumable biomass in saline areas where non-halophytic species cannot grow or have low dry matter yields. Therefore, halophytes and some other salt-tolerant plants can provide a drought reserve or a supplementary feed source under arid and semi-arid conditions. On grazing lands, the halophytes can serve as a complementary nutrients source to other conventional feedstuffs, such as Atriplex spp. and cereal straws or hays. In addition to biomass production, wide variations in palatability, chemical composition, nutritive value and animal responses to several halophytes and salt-tolerant forages have been reported in the literature. Some of these species could be valuable sources of minerals and or nitrogen. However, the provision of energy supplements (e.g. barley) is necessary to overcome maintenance and or moderate production requirements of sheep and goats fed on halophytes and or salt-tolerant forages-based diets. Many studies showed that these plants could be used advantageously as alternative feeds to replace totally or partially common feedstuffs, thus to alleviate feeding cost. However, the presence of high contents of ash, plant secondary metabolites and non-protein nitrogen (NPN) should be taken into consideration when formulating diets containing halophytes and or salt-tolerant forages for small ruminants. Although most of feeding studies reported in this review have been carried in the Near East region, mainly in Egypt, results obtained in other regions worldwide support that feeding salt-tolerant plants and halophytes could promote livestock production systems, increase farmers’ incomes and improve environmental conditions in the saline areas. © 2010 Elsevier B.V. All rights reserved.

1. Introduction Populations in the developing countries are growing so quickly that the arable lands and the available fresh water are unable to sustain them. It was estimated from the various available data that globally the world is loosing at least 3 ha of arable land every minute because of soil

夽 This article is part of the special issue entitled “Potential use of halophytes and other salt-tolerant plants in sheep and goat feeding” guest edited by H. Ben Salem and P. Morand-Fehr. ∗ Tel.: +20 10 2588988. E-mail address: drc [email protected]. 0921-4488/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2010.01.010

salinity (Anon., 2006). Halophytes and other salt-tolerant plants may provide sensible alternatives for many developing countries (Squires and Ayoub, 1994). These plants can grow in saline to extremely saline habitats and have particular characteristics which enable them to evade and/or tolerate salinity by various eco-physiological mechanisms. These plants are naturally grown or cultivated in saltaffected lands such as in saline semi-deserts, mangrove swamps, marshes, sloughs, degraded soils and seashores. The vegetative yields of halophytes and other salt-tolerant plants species could have great potentialities particularly as sources of livestock fodders (Anon., 2009). There are many halophytes and salt-tolerant shrubs, grasses and legumes which could be established in saline lands for

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H.M. El Shaer / Small Ruminant Research 91 (2010) 3–12

feeding livestock (e.g. Kochia sp., Juncus sp., Leptochloa fusca, Acacia sp., Suaeda fruticosa, Nitraria retusa, Salsola sp., Atriplex sp., Paspalum distichum and Scirpus litoralis). The fodder quality of these plants depends on a combination of climatic, soil, and plant factors. Halophytes have the advantage of tolerating high salt levels in the saline lands and have economic potentialities in the arid and semi-arid areas (Zahran, 1993; El Shaer, 1999). However, the value of certain salt-tolerant forage crops has been recognized by their incorporation in the rangelands improvement programs in many salt-affected regions throughout the world. Although economic consideration of halophytes and other salt-tolerant plants is just beginning, they are now receiving increased attention particularly in arid regions where salinity problems are very crucial. Bearing in mind that the fodder potential and or animal responses to some common halophytes and salt-tolerant plants (e.g. Atriplex spp., Kochia spp., Sorghum) will be addressed in detail in the other review and original articles of this special issue by authors from other regions, we summarize in this paper the main information on the potential use of a wide range of halophytes and other salttolerant forages which was evaluated mostly in the Near East region, particularly in Egypt. After reviewing production potential of halophytes and some other salt-tolerant plants, we discussed literature data on their nutritive value, on animal performances fed on these feed resources and the main constraints hampering the efficient integration of these halophytes and salt-tolerant plants in livestock feeding calendars. 2. Halophytes and salt-tolerant fodder production Halophytes and salt-tolerant plants have been used as feed resources in arid and semi-arid regions for millennia (Le Houérou, 1993; Glenn et al., 1999; El Shaer, 1999; El Shaer et al., 2005). Many of the halophytic plant species and salt-tolerant fodder species provide a valuable reserve feed for grazing animals particularly under drought conditions or fill regular gaps in feed supply caused by seasonal conditions. The value of certain halophytic shrubs, legumes and grass species has been recognized by their incorporation in pasture improvement programs in many salt-affected regions throughout the world (Glenn et al., 1999; ICBA, 2006). There have been recent advances in selecting species with high biomass and protein levels and the ability to survive a wide range of environmental conditions including salinity (Anon., 2009). Among the potential selected salt-tolerant species are: (i) From Leguminosae: Acacia ampliceps (Salt wattle acacia), Acacia cyanophylla, Sesbania sesban (Sesban) and Cajanus cajan (Pigeon pea), and (ii) From Graminae: Cenchrus ciliaris (Buffel Grass), Panicum maximum Jacq (Guinea grass), P. maximum var. trichoglume (Green panic), Pennisetum americanum (Pearl millet), Sorghum bicolor (Sorghum), and Sorghum sudanense (Sudan grass). Moreover, halophytic grasses, e.g. Sporobolus virginicus, Distichlis spicata, Paspalum and Kallar grass, showed excellent growth performances under different salinity treatments (ICBA, 2006). Pearl millet (Pennisetum glaucum, L. R. Br.), Sudan grass (S. sudanense) and Sorghum (S. bicolor, L. Moench) are

Table 1 Productivity of some halophytes in Mexico (O’Leary, 1984). Species

Productivity (g DM/m2 /year)

Atriplex lentiformis Batis maritima Atriplex canescens subsp. Linearis Salicornia europaea Atriplex barclayana Atriplex nummularia

1794 1738 1723 1539 863 801

among the most potential salt-tolerant grass species as good quality fodders for small ruminants in Egypt and other countries in the Near East (Anon., 2009). In late 2004, the International Center for Biosaline Agriculture (ICBA), Dubai, UAE, partnering with the International Fund for Agricultural Development (IFAD) and the Social Fund for Economic and Social Development (AFESD) and some research centers in seven countries in the Near East region began a 4-year project. The overall goal of the project was to improve livelihood and income of the local poor people in such countries by introducing salt-tolerant fodder crops and management practices, under utilized marginal lands and saline water. According to the report of ICBA (2006), many genotypes including germplasm accessions, breeding lines hybrids and commercial cultivars were highly suitable and widely accepted by farmers due to their high production and nutritive value. Furthermore, Sorghum, Pearl millet, C. ciliaris, Panicum turgidum grasses and fodder beet as an example, perform well in salty soils. Genotypes of the same plant species could have different biomass yields. Many plant species growing on saline lands can produce high to moderate consumable biomass (Zahran, 1986; Le Houérou, 1994; El Shaer, 1999; El Shaer et al., 2005). According to ICBA (2006), at 20 dS/m, the fresh yield of Atriplex lentiformis, Atriplex nummularia and Atriplex halimus reached nearly 25.0, 16.9 and 14.6 t/ha. Higher biomass yields were obtained with some salt-tolerant crops like Sporobolus (29 t/ha). In Mexico, O’Leary (1984) evaluated the productivity of some selected halophytic crops under irrigation using highly saline irrigation water (40,000 mg/l sea water). A. lentiformis, Batis maritima and Atriplex canescens performed better than the other halophytic plants (Table 1). Some grass species such as Puccinellia stricta, tall wheat grass (Thinopyrum ponticum) and a mixture of clover (Trifolium michelianum) and Italian ryegrass (Lolium multiflorum) cultivated under moderate to high salinity conditions yielded 12.2, 5, and 2 t/ha, respectively (Warren et al., 1996). Some other halophytes (e.g. Hammada elegans, Thymelaea hirsute, Tamarix sp., N. retusa, Salsola sp.,) and other salt-tolerant plants (i.e. A. cyanophylla, Kochia spp.) may have low edible dry matter yields and cannot support significant animal production (El Shaer, 1981; Zahran, 1993; Le Houérou, 1994). Growing a combination of salt-tolerant grasses (such as Guinea grass, Green panic, Pearl millet, Sorghum, and Sudan grass), legumes (i.e. S. sesban, Sesban and C. cajan) and some Atriplex species would improve the feeding value of dietary rations, and animal production on saline lands (Anon., 2009). Numerous salt marsh plant species can be used as fodder crops under saline conditions of semi-arid and arid

H.M. El Shaer / Small Ruminant Research 91 (2010) 3–12

regions. Economic studies indicated that farmers are making money from saline wasteland (Salerian et al., 1987; Malcolm, 1993). The extension of halophytes and other salt-tolerant plants into farming practice will depend on their compatibility with the current land use system. It depends also on the farmer acceptance and on the provision of adequate incentive to encourage pasture and forage crop production. 3. Feeding and nutritional value of halophytes and salt-tolerant fodder crops Some data and information related to the nutritional value of halophytes and salt-tolerant fodder crops are briefed in the article and focused mainly on dominant plant species in the Near East region. It is worthy to note that halophytes and other salt-tolerant plants can constitute a major part of the feeding program of sheep, goats, camels and some wildlife animals in the arid and semiarid regions (Squires and Ayoub, 1994; El Shaer, 1997). The most dominant halophytes, based on their distribution and coverage, in the Near East region are Alhagi maurorum, Arthrocnemum macrostachyum, Arthrophytum scoparium, Atriplex spp., Avicennia marina, Haloxylon salicornicum, Halocnemum strobilaceum, Juncus spp., Limonium monopetahum, L. fusca, Kochia spp., N. retusa, Tamarix spp., Salsola spp., Suaeda spp. and Zygophyllum spp. Wide intraand inter-plant species variations in productivity, palatability, chemical composition, and nutritive value of several halophytes and salt-tolerant forages have been reported in the literature. These variations depend on seasonal changes, environmental conditions and management practices (Abd El Aziz, 1982; Gihad and El Shaer, 1994; Le Houérou, 1994; Abd El-Rahman, 1996; El Shaer, 2004). Climate factors, i.e. temperature, humidity precipitation and light intensity play an important role in controlling the nutrient contents and nutritive value of plants as they affect assimilation, photosynthesis and metabolism. Data, derived from many studies, on average values of chemical composition, fiber constituents and dry matter digestibility (DMD, %) of most dominant halophytes in the Near East region are summarized in Table 2. As percentages of dry matter, chemical constituents, acid detergent fiber (ADF), acid detergent lignin (ADL), neutral detergent fiber (NDF) and DMD varied considerably among forage species. These plants attained a wide range of crude protein content (CP) varying from 3.38% DM (Alhagi glaucum) to 15.1% DM (Atriplex leucoclada) and, generally, most of these plant species attained reasonable CP and high ash contents as a character for salt marsh plants. Digestibility of halophytic range species, on dry matter or on organic matter basis, may vary greatly with plant species, phonology and season; it may reach 70% under the best conditions and drop below 40% in unfavorable circumstances (Le Houérou et al., 1982, 1983; Le Houérou, 1993). Furthermore, such rangelands are usually fairly poor in energy and high in CP (Le Houérou, 1981; Benjamin et al., 1992). The available net energy (NE) is typically 2.5–4.0 MJ/kg DM and metabolizable energy (ME) ranges between 5 and 8 MJ/kg DM, i.e. 0.36–0.57 Scandinavian Feed Units/kg DM or 0.25–0.40 kg TDN/kg DM (Le Houérou, 1981, 1993). The energy range in halophytes is

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thus 50–60% of the energy value of common fodder crop roughage while CP content ranged from 8 to 20% DM. However, as mentioned above, less than 50% of these nitrogen compounds are true digestible protein (Yaron et al., 1985; Benjamin et al., 1992). It is reported that fibrous materials and ash contents of halophytic feed materials are higher and increase while gross energy and protein contents are low and decrease with advancing maturity (Kandil and El Shaer, 1988). Therefore, most of halophytes are nutritious in wet seasons and can overcome maintenance requirements of animals whereas they are low in nutrients in summer and autumn (dry season) and need to be supplemented with other feed ingredients, particularly with energy feed resources (El Shaer, 1997; Atiq-ur-Rehman, 2002). Based on data in Table 2, it seems that most of naturally grown halophytes could cover the essential nutrients for maintenance requirements of small ruminants in good rainy seasons according to the recommended nutritional requirements of livestock in the Near East region as indicated by Kearl (1982). It was reported that differences between plant species and genera may be larger especially in their chemical composition and dry matter and organic matter digestibility (Le Houérou, 1994; El Shaer, 1999). The CP content of both A. halimus and A. nummularia was 10% higher than A. lentiformis (ICBA, 2006). The nutritive value of six halophytic shrubs (Acacia saligna, A. nummularia, A. semibaccata, A. halimus, P. distichum and S. litoralis) naturally grown in the Mediterranean coastal zone in Egypt was evaluated by Zahran (1993). Nutrient contents varied among all halophytic plants including Atriplex spp. Most of these plants were high in CP such as A. nummularia and S. litoralis (18.2 and 17.8% DM, respectively) but all of them contained enough amounts of nitrogen to cover the requirements for the rumen microflora (Van Soest and Jones, 1968). In general, A. saligna, A. nummularia and A. semibaccata seemed to be nutritious based on their moderate nutritive value which can meet the maintenance nutritional requirements for ruminants (Kearl, 1982). The salt marsh plants are relatively high in most of major minerals without any risk for animal health (Gihad and El Shaer, 1994; Abd El-Rahman, 2008). However, some halophytes are deficient in sulphur and phosphorus (El Shaer, 1981). Furthermore, there is no trace elements deficiency or toxicity observed for most of halophytic species (Le Houérou, 1994; Gihad and El Shaer, 1994). Variation of palatability rates of some halophytes naturally grown in Egyptian deserts was detected using different techniques such as esophageal fistulae technique (El Shaer, 1981; El Shaer et al., 1990) and regular daily field observations during the wet and dry seasons of the year (Zahran, 1993; El Shaer, 1999; Abd El-Rahman, 2003). As indicated in Table 3, some plants are non-palatable for goats and sheep but they are slightly palatable for camels in both wet and dry seasons such as Suaeda spp., H. strobilaceum and Zygophyllum album. The palatability rate of Salsola tetrandra, N. retusa and A. halimus varies from wet to dry season. S. fruticosa, N. retusa and S. tetrandra could represent the most important shrubs due to their high palatability for all animal species, in addition to their

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H.M. El Shaer / Small Ruminant Research 91 (2010) 3–12

Table 2 Chemical composition (% DM basis) and dry matter digestibility (%) of most dominant halophytes. Plant speciesa

DM

CP

EE

CF

Ash

NFE

NDF

ADF

ADL

DMDb

Alhagi maurorum Arthrocnemon glaucum Atriplex canescens Atriplex halimus Atriplex leucoclada Atriplex nummularia Atriplex semibaccata Halocnemum strobilaceum Haloxylon salicornicum Hamada elegans Juncus acutus Kochia indica Limoniastrum monopetalum Nitraria retusa Salcornia fruticosa Salsola kali Salsola tetrandra Salsola vermiculata Suaeda fruticosa Tamarix aphylla Tamarix mannifera Thymelaea hirsuta Zygophyllum album Zygophyllum simplex Zygophyllum decumbens

44.0 22.9 32 34.2 25.6 21.7 34.0 29.7 42.2 24.1 35.0 30.5 48.6 37.6 37.6 89.8 37.1 45.0 25.0 34.9 40.0 42.6 24.7 40.5 37.7

9.4 3.4 14.2 12.6 15.1 13.3 14.0 6.7 14.8 7.8 7.1 14.0 11.5 10.2 13.5 15.0 6.3 8.1 10.0 12.9 8.2 8.2 7.8 11.1 9.4

4.4 1.3 4.1 2.3 2.7 5.1 3.6 2.2 6.1 3.9 2.3 2.8 3.5 2.5 1.9 2.0 2.4 3.8 5.0 4.0 3.6 4.3 2.5 2.1 1.8

29.5 12.1 18.3 25.4 27.4 24.2 20.6 17.0 24.1 26.5 28.5 30.2 14.6 32.6 18.9 24.9 36.1 33.9 33.2 13.6 11.6 31.4 11.2 16.7 24.1

25.9 31.9 19.6 22.7 31.7 26.7 17.5 40.3 15.9 24.6 12.3 15.1 23.6 33.0 14.3 12.2 35.9 25.2 16.1 20.1 24.9 17.9 34.2 29.8 26.9

30.7 51.4 43.8 37.0 23.1 30.7 44.3 33.8 39.1 37.2 49.9 37.9 46.8 21.7 51.4 44.9 19.3 29.0 35.7 49.4 51.7 38.2 44.4 40.3 37.8

50.3 48.9 34.5 64.6 36.9 46.3 46.9 68.2 58.4 46.6

34.4 35.9 28.7 40.2 29.1 27.3 28.1 39.6 37.1 38.6

13.1 11.2 11.3 10.4 11.0 7.2 9.0 12.1 10.1 11.7

62.1

39.4

12.0

38.8 37.4 38.0 39.7 40.1 33.7 36.0 50.7 58.9 35.6 40.7

29.0 31.1 30.1 30.0 33.3 22.3 26.0 31.2 35.0 23.6 30.1

10.2 9.11 10.5 12.9 10.7 12.0 12.4 13.5 17.3 6.70 12.1

46.4 50.4 57.8 56.7 52.2 57.2 58.3 36.9 46.5 53.6 34.4 67.9 55.5 61.8 60.5 64.5 60.0 60.4 70.4 59.6 65.3 47.1 56.9 49.6

a b

Data cited from El Shaer (1981); Abd El Aziz (1982); Abd El-Rahman (1996); El Shaer and Zahran (2002); Gihad et al. (2003). DMD%: in vitro dry matter digestibility (%).

moderate nutritive value, particularly during the wet season. These shrubs are often overgrazed during winter and spring seasons in particular S. fruticosa and therefore, they should be managed to maintain regrowth (El Shaer, 1981, 1997).

Like non-halophytic forages, most of halophytic forages are high in nutrients and are palatable during early growth stages, whereas the opposite is true during late stages of growth (El Shaer, 1981; Le Houérou, 1993). Some plant species mature rather rapidly and

Table 3 Chemical composition (% DM) and palatability index of dominant halophytic range plants in Egypt. Plant speciesa

DM

CP

CF

EE

Ash

Sheep

Camel

40.5 31.5

NP NP

NP NP

PP PP

26.5 28.5

49.4 47.3

NP NP

NP NP

PP PP

2.2 1.8

26.0 30.9

48.0 43.5

PP PP

PP NP

FP FP

12.4 14.4

2.6 1.7

30.1 35.8

45.1 39.7

FP PP

FP PP

HP HP

9.1 7.2

12.8 18.2

3.0 2.3

16.2 19.7

58.9 52.6

HP PP

HP FP

HP HP

42.1 58.4

9.2 6.3

18.7 22.6

3.2 3.1

31.4 36.7

37.5 31.3

FP PP

FP PP

HP FP

30.9 48.3

11.1 8.4

10.9 13.7

3.9 3.0

25.4 30.3

48.7 44.6

HP FP

HP HP

HP HP

6.8 4.2

14.6 19.6

2.5 2.2

35.7 42.5

Zygophyllum album Wet season Dry season

30.4 39.3

7.1 6.3

14.6 16.2

2.2 1.6

Tamarix mannifera Wet season Dry season

57.4 63.1

7.6 6.3

16.1 17.5

Salsola tetrandra Wet season Dry season

45.0 49.9

9.7 8.4

Nitraria retusa Wet season Dry season

14.6 20.1

Atriplex halimus Wet season Dry season Suaeda fruticosa Wet season Dry season a

Palatability indexb (%) Goat

Halocnemum strobilaceum Wet season 28.6 Dry season 37.8

b

NFE

Data cited from El Shaer (1981, 1999); El Shaer et al. (1990). PI, palatability index: HP, highly palatable; FP, fairly palatable; PP, poorly palatable; NP, non-palatable.

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consequently their nutritive value was substantially decreased; other species mature rather slowly and consequently remain high in nutrients over an extended period. Chemical composition of some dominant halophytes in Sinai, Egypt was determined during wet season (winter and spring) and dry season (summer and autumn). The main results obtained by El Shaer (1981, 1999) and El Shaer et al. (1990) are summarized (on average basis) in Table 3. All nutrients are influenced by advancing season of growth. For example, the levels of CP, EE and NFE decreased whereas CF, ash and DM contents increased on passing from the wet season to the dry season. The authors, also, reported that with advancing maturity of halophytes, the contents of silica, cell wall constituents (CWC), cellulose and lignin increased while CP, phosphorus and gross energy decreased. Moreover, the process of aging and maturation was associated, also, with a decline in DM digestibility (DMD), organic matter digestibility (OMD) and CP digestibility. The reduction in the rate of digestibility associated with aging is likely due to the increase of the proportions of structural to non-structural carbohydrates. Supplementary feeding, particularly with energy supplements, is recommended for small ruminants grazing such halophytes during dry seasons and prolonged drought period (El Shaer, 1981). The effect of growth stages of cultivated A. nummularia on its nutritive value was determined using sheep and goats in Egypt (Kandil and El Shaer, 1990). It was concluded that the plant was more nutritious in the spring and winter seasons than in summer and autumn seasons. Intake, digestibility coefficients and nitrogen balance were significantly affected by advancing maturity of A. nummularia. Photosynthetic products are more rapidly converted to structural compounds, these results in decreased protein and soluble carbohydrates and increased structural cell wall contents in summer. The authors also, stressed the necessity of supplementary feeding with energy sources during dry seasons to provide livestock with essential nutrients for their production, particularly during late pregnancy and mid lactation. Some salt marsh plants, in particular chenopods forages, are relatively low in metabolizable energy (0.5–0.7 MJ/kg DM; equivalent to a net energy of 2.5–3.5 MJ/kg DM), but could overcome the maintenance requirements of sheep when DM intake ranges from 1.2 to 1.5 kg/day during rainy seasons (Le Houérou, 1994). The nutritive value of six salt-tolerant grasses growing in saline lands of North Sinai, Egypt and irrigated with saline ground water (7000 ppm total salts) (was evaluated by El Shaer et al. (1987). Most of these grasses were well adapted to the area saline conditions. They contain sufficient nutrients that may cover the ruminant requirements. Napier grass (Pennisetum purpureum, Elephant grass) and green panic grass (P. maximum var. trichoglume) attained the highest nutritive values (El Shaer et al., 1987). It is worthy to mention that these grasses in addition to Rhodes grass (Chloris gayana) and Buffel grass (C. ciliaris) have been extensively grown in several salt-affected areas in Egypt for feeding cattle and small ruminants. On the other hand,

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the nutritive value of Kochia indica, Juncus subulatus and L. fusca cultivated in salt-affected lands in the Mediterranean Coastal zone of Egypt were compared to clover hay, for their fodder potential (Zahran, 1993). Concerning K. indica, a slightly high digestion coefficient of DM (61%) was recorded while the TDN was relatively low (46.9%); probably due to the high ash content of this plant species. The low nitrogen retention in Kochia is most likely a function of less efficient utilization of absorbed nitrogen which in turn was influenced by high urinary nitrogen excretion (14.7 g/day). J. subulatus and L. fusca contained comparable amounts of DM (30.0 and 35.0%), organic matter (89.6 and 88.5%), EE (1.7 and 2.2%), nitrogen-free extract (47.2 and 49.4%), CP (16.1 and 8.7%) and ash (10.4 and 11.6%). The TDN and DCP of the two plants were 57.21, 10.72% and 53.73, 5.64%, respectively. These forages are nutritious fodders that would cover the nutritional requirements of livestock (Kearl, 1982). Nevertheless, grazing potentialities of such cultivated halophytic plant species were observed on the saline lands in Egypt, where sheep, goats, cattle and donkeys were freely allowed to graze for two months without any symptoms of toxicity (Zahran et al., 1999; El Shaer and Zahran, 2002) and look in good health. It seems that such plant could be successfully cultivated in saline soils and irrigated with saline well (under ground water) to produce alternative feed materials. Recently, three salt-tolerant grasses (Sudan grass, Pear millet and Sorghum grass) were cultivated in salt-affected soil of South Sinai Research Station, Egypt and were irrigated with ground saline water (averaged 7000 ppm total salts) as reported in Anon. (2009). The grasses appeared to be nutritious for small ruminants as it contained moderate concentrations of CP (averaged 13.6, 13.6 and 13.5% for Sudan grass, Pear millet and Sorghum grass, respectively) to cover their protein requirements. In addition, they attained high content of organic matter (86%) with low concentrations of ADF and ADL (ca. 30 and 4% for Sudan grass; 33 and 5% for Pearl millet; 28 and 3% for Sorghum grass, respectively). Such grasses have great potentialities for feeding sheep and goats during summer and autumn seasons which coincides with feed shortage and increased prices of conventional feed materials (Anon., 2009).

4. Effect of feeding halophytes and salt-tolerant plants on livestock performances The effect of feeding salt-tolerant forages and halophytic feed materials, as sole diets or incorporated with traditional feed ingredients, on small ruminants and camels performances was investigated in some countries in the Near East region (i.e. Egypt, Tunisia, Iran, Israel, Syria and UAE) during the last two decades. The review focuses on the Egyptian experiences as an example. There have been numerous research and on-farm studies, conducted since early eighties mainly at the Desert Research Center in Egypt, on sheep, goats and camels fed on halophytes and salt-tolerant plant species. The main findings of such studies are, briefly, discussed herein.

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4.1. Effect of feeding halophytes and salt-tolerant plants on sheep and goats performance The effect of energy supplements on pregnant and lactating sheep and goats grazing natural halophytes in Sinai, Egypt, and supplemented with different levels of barley during two successive years was evaluated by El Shaer (1981). It appeared that both animal species could not sustain themselves on the natural range species solely without barley supplementation. The author reported that barley provision (350 g/head/day) improved (P < 0.05) the DM and nitrogen intakes of the range species during the wet (winter and spring) and drought seasons (summer and autumn). The performance of grazing dams during the pregnancy and lactation stages, in terms of body weight changes and milk yield, in addition to daily gain and weaning weight of their offsprings were improved (P < 0.05) by the energy supplementation. Therefore, additional supplements are needed for productive animals grazing halophytic pastures. Similar trends were reported by El Shaer and Kandil (1990) who recommended the supplementation of soluble carbohydrate source (e.g. barley, corn, ground date stones and molasses) to improve the performance of sheep and goats fed salt-tolerant forages. Daily amounts of 150 and 250 g barley/head were recommended by the authors for sheep fed saltbush during wet and dry seasons, respectively. The inclusion of a supplement, particularly a soluble carbohydrate source, to the diet of sheep or goats fed on saltbushes increased its intake, digestibility and growth rate (El Shaer and Kandil, 1990). The impact of feeding halophytes on performance and carcass traits of goats was investigated by Youssef et al. (2002). A combination of halophytes, grown naturally at the Red Sea Coast, Egypt, namely Tamarix mannifera, Halocnemum strobilacum and Z. album were supplemented with concentrate feed mixture and fed to goats as hay in comparison with berseem (Trifolium alexandrinum) hay as a control diet. The authors reported that the goat kids fed Berseem hay had higher daily gain (90 g/day) than those fed the halophytic mixture (80 g/day) and dressing percentage based on fasting weight were 46.9 and 44.5%, respectively. Dressing rates (53.4% vs. 52.8%) were comparable (P > 0.05) in kids receiving both diets. The same authors, in another trial, recommended that a diet composed of A. saligna and concentrate mixture was efficient for fattening kids without significant differences in carcass characteristics compared to traditional fattening diets. Furthermore, feed intake and efficiency, average daily gain, nutrient digestibility and retention for lambs fed chopped green K. indica compared to Berseem hay (T. alexandrinum, as a control diet) were determined in feeding trials conducted by Fahmy and Ibrahim (2005). Digestibility of DM, CP, CF and EE and nutritive values were greater for K. indica diet than those of Berseem hay diet. Nitrogen balance of lambs fed K. indica diet was higher (P < 0.05) than that of Berseem hay diet. Average daily gain and feed efficiency were similar between the two diets but feeding costs of K. indica diet was less than that of Berseem hay diet. It was recommended that K. indica could replace Berseem hay (as good quality traditional hay) for feeding lambs. Furthermore, A. saligna and A. halimus supplemented with

barley could be used successfully and safely for kid and lamb fattening without adverse effects on their growth performance and meat characteristic (Shehata and Mokhtar, 2005). The results, also, showed that dressing rate differed (P < 0.01) between the two animal species (44.2, 41.6% and 51.5, 49.6% for lambs and kids, respectively). Also, the dressing rate of slaughtered animals and their empty body weights differed with the halophyte species included in the diet (i.e. Acacia vs. Atriplex groups, (43.6 vs. 42.2% and 51.4 vs. 49.7%, respectively). 4.2. Effect of feeding halophytes and salt-tolerant plants on camel performance Some studies have been carried out on camels fed some halophytes in Egypt. Experiments on fattening camel on A. halimus with different energy sources were conducted to evaluate growth performance, efficiency of feed utilization and carcass traits of male calves (Shawket and Safinaz, 1999). Daily intakes of DM, TDN and DCP were not affected by the experimental diets. At the same time, feed conversion, in terms of kg TDN/kg weight gain and kg DCP/kg gain, of calves fed saltbush and barley only or with olive cake was greatly improved. The author concluded that feeding camel calves on fresh saltbush resulted in a substantial reduction in the feeding cost for producing 1 kg body weight. Additionally, the dressing percentage and boneless meat percentage for yearling male camels were not affected by diet composition. The results clearly showed that fresh saltbush can be successfully and economically used in feeding camel calves in arid and semi-arid zones. Furthermore, fresh A. nummularia and A. saligna were supplemented with both ground date stone and olive cake and fed to young male camels in a fattening trial to evaluate their growth performance and carcass yield (Shehata et al., 2004). The results indicated that daily intakes of halophytic shrubs differed significantly among the different groups. Slaughter body weight, empty body weight, hot and chilled carcass weights were similar among the different camel groups. It was noticed that the dressing percentages of camels fed A. nummularia were the lowest (59.7 and 68.1%). It was concluded that feeding male camels on such halophytic fattening diets, in particular A. saligna ration, reduced the feeding costs required to produce 1 kg gain compared to the conventional rations. The authors recommended that the use of concentrate mixture plus edible parts of the halophytic plants in feeding growing camels during 8 months would improve economical efficiency of meat production under arid and semi-arid conditions with no adverse effects on their whole sale cuts, physical components, and fat deposits, sensory, physical and chemical characteristics of camel meat. 5. Constraints to feeding halophytes and salt-tolerant plants The low palatability, consumption and nutrients utilization of some halophytic species and salt-tolerant forages could be attributed to many factors such as ash content, lignification, plant secondary metabolites and non-protein nitrogen (NPN) content.

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5.1. Ash content Most of halophytes are characterized by high ash content, mainly Na, K, Ca and silica (El Shaer, 1981; Bayoumi et al., 1990; Le Houérou, 1993; Abd El-Rahman, 2008). As stated by Masters et al. (2001), sheep can tolerate a sodium chloride intake in feed of about 100–150 g/day provided that they have access to a non-saline drinking water. It means that the high level of dietary salt will act to reduce feed consumption. Similar findings were reported by (Hamilton and Webster, 1987); the high Na and K content may limit feed intake and reduce digestibility by shortening rumen turnover times (Le Houérou, 1981, 1993; Rossi et al., 1998). High salt content is perhaps the major negative component in Atriplex species. Sodium levels could be higher than 8% DM. Therefore, mixing some saltbushes with low salt forages is desirable (ICBA, 2006; Anon., 2009) and recommended for better utilization of saltbushes. Moreover, offering fresh drinking water to animals fed saltbush would reduce the stress of salt intake and also enhance saltbush consumption and nutrients utilization (El Shaer, 1999). 5.2. Lignification factor Halophytic plants vary greatly in their contents of crude fiber (CF) contents and fiber constituents such as NDF, ADF, ADL, cellulose and hemicellulose as summarized in Table 2. Many halophytes and salt-tolerant plants contain high fiber concentration which reduces digestibility of most nutrients (Van Soest and Jones, 1968). The low intake and poor utilization of many halophytic species may be associated mainly with the degree of cell wall constituents (CWC) digestion (Van Soest and Jones, 1968; El Shaer et al., 1990; Abd El-Rahman, 2008). Within plant species, significant negative correlation usually exists between forage lignin content and either forage DM intake or nutrient utilization as reported by El Shaer (1981); Le Houérou (1994) and Abd El-Rahman (1996). In this regard, forage characteristics which may affect voluntary intake and utilization are (i) the content of digestible CWC, (ii) the content of indigestible CWC, (iii) the structure of CWC, and (iv) the content of cytoplasmic constituents. On the other hand, high levels of ADL and NDF have been considered the most remarkable factors which limit forage intake and digestibility (Van Soest and Jones, 1968; Le Houérou, 1993). The content of CF or fiber constituents in forage plays an important role in its selection by livestock. Forages with high fiber content are usually better accepted by cattle than by sheep and goats; but this, in turn, depends on the proportions of the various components of fiber, i.e. cellulose, hemicellulose, ADF, NDF, etc. 5.3. Plant secondary metabolites The anti-nutritional factors (ANFs) or secondary metabolites are natural chemical metabolites produced and biosynthesized by plants and may be acutely or chronically toxic to animals causing major economic losses to livestock producers Most halophytes contain various concentrations of different ANFs (e.g. tannins, saponins,

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alkaloids and nitrates) which have significant impact on their utilization as feed materials (Gihad et al., 2003; El Shaer et al., 2005; Abd El-Rahman, 2008). As reported by Batanouny (1996), several natural or introduced Mediterranean halophytic shrubs and trees have high contents of tannins, in particular A. cyanophylla Lindl. (Syn. A. saligna). Tannins, as polyphenolic compounds, could be detrimental or beneficial for animals depending on their concentrations in the feed materials. The incorporation of low levels of tannins (2–4%) in the diet increased the proportion of protein escaping rumen degradation and the absorption of essential amino acids whereas higher tannin levels (4–10%) decreased forage intake (Terrill et al., 1992; Barry and McNabb, 1999). Tannins may interfere with proteins availability to animals and this could affect negatively other productive traits of small ruminants such as growth rate, feed intake and nutrient digestibility (Kumar and Vaithiyanathan, 1990; Ben Salem et al., 1999; El Shaer et al., 2005) and wool growth and reproduction (Kumar and Vaithiyanathan, 1990). The presence of these compounds in some halophytes forms insoluble complexes with essential minerals, proteins and carbohydrates, lowering the nutritive value of the product. The use of polyethylene glycol (PEG), a synthetic polymer, proved efficient in deactivating tannins (Ben Salem et al., 1999) hence improving the efficiency of utilisation of several shrubs-containing-tannins by animals (Makkar, 2003). Several halophytes and salt-tolerant plants (i.e. fodder beet) contain various concentrations of oxalates and nitrates which vary according to plant species and season of the year (Gihad et al., 2003; El Shaer et al., 2005). Oxalates cause precipitation of insoluble calcium oxalate in the rumen and kidneys leading to calcium deficiency, kidney damage and finally causing possible death. Hungerford (1990) concluded that poisoning in sheep and cattle has been reported when pastures contain 7–8% oxalates. It is worthy to mention that many chenopods contain oxalates levels approaching the toxic threshold. Oxalates concentrations ranging from 3.3 to 6.6% DM were found in the leaves of five different Atriplex spp. grown on one area (Malcolm et al., 1988) whereas higher values have been reported in young plants from the same species (Davis, 1981). Despite these reports, toxicity is not a common observation (Atiq-ur-Rehman, 1995), possibly because the high oxalate concentrations can decrease plant material intake as reported by Burritt and Provenza (2000) who indicated that 3% oxalates depress intake significantly. Some Kochia spp. such as Kochia scoparia is liable to oxalate toxicity when this forage proportion exceeds 40% of the diet for a long time, as this forage may contain 3–7% oxalates on DM basis (Sherrod, 1973). Nitrates are converted to nitrites in the rumen leading to the conversion of hemoglobin to methaemoglobin that causes anoxia accompanied by increased pulse and respiration rates. It is reported that toxic levels of nitrogen as nitrates are above 5000 mg N/kg DM in the diet (National Research Council, 1974). Burritt and Provenza (2000) found that 8000 mg N/kg DM reduced feed intake in sheep by over 60%. The effect of season of the year on chemical composition and some ANFs of six halophytic species fed

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to Barki sheep as fresh, silage, haylage and hay materials in Egypt was evaluated (El Shaer et al., 2005). The halophytes were A. saligna, A. nummularia, Arthrocnmum glaucum, H. strobilaceum, T. mannifera and Z. album. The content of ANFs of these species varies greatly with plant species and seasons. The authors, also, found that tannins concentrations were high in all plant species, particularly in autumn season; A. saligna showed the highest concentration (12.38 mg/100 mg DM) during all seasons of the year, while A. nummularia attained the lowest value (6.33 mg/100 mg DM). Regardless the plant species, maximum values of flavonoids and oxalates were recorded in winter (2.9 ␮g/100 mg and 4.9 mg/100 mg DM, respectively), while the minimum values were recorded in summer (1.9 ␮g/100 mg DM and 3.4 mg/100 mg DM, respectively). The concentrations of oxalates in spring, autumn and winter were comparable for all plant species. The authors recommended that these halophytes should not be offered to animals as fresh material, particularly in the spring season as most of these plants are high in ANFs. The processing methods strongly affected the concentrations of ANFs in the studied shrubs. Feeding the processed halophytic materials to small ruminants in the form of silage and haylage improved their feed intake and consequently enhanced their body weight gain. 5.4. Non-protein nitrogen (NPN) content Some halophytes, particularly the chenopod species, contain reasonable CP level (Table 2) which could cover N requirements of grazing animals. The nitrogen richness of such plants may not be fully used by ruminants since non-protein nitrogen (NPN) represents about 50% of this nitrogen (Abd El Aziz, 1982; Le Houérou, 1993). The NPN could not be retained and metabolized unless an appropriate energy source would be available for the proliferation of rumen microorganisms (Le Houérou, 1994). Therefore, animals accustomed to halophytes have adapted rumen microflora which can use the NPN of diets high in energy or supplemented with energy sources (e.g. barley and molasses) (El Shaer, 1981; Le Houérou, 1994). However, the nutritive value and palatability of halophytes or salt-tolerant foragers that contain any of the above mentioned four factors might be improved through applying specific one or two treatments like physical treatments (e.g. chopping, soaking and sun-drying), chemical treatments (e.g. PEG) and biological treatments (e.g. ensiling). These treatments could reduce the concentrations of secondary metabolites, ash content and/or affect the ligno-cellulose bonds (El Shaer et al., 1990, 2005; Abd El-Rahman, 2003; Youssef et al., 2003; Anon., 2009). Furthermore, Masters et al. (2001) stated that a mixture of salt-tolerant grasses, legumes, shrubs and forbs maximizes the feeding value of the pasture. It could be an appropriate solution to enhance the utilization of halophytic fodders. Such mixture would offer to grazing animals the opportunity to select specific plants. For example, grasses, legumes and chenopods have different compositions of salt, anti-nutritive factors, fiber and nitrogen, thus they could have complementary roles in livestock feeding. Sim-

ilar approaches have been applied, nowadays, in some countries in the Near East region (i.e. Egypt, Morocco, Tunisia, Oman, UAE, Jordan, Syria and Palestine) in cooperation with ICBA projects (ICBA, 2006; Anon., 2009). As expected, sheep fed on A. nummularia only performed poorly and had the lowest growth rates while those fed Rhodes grass had the highest average daily gains (ICBA, 2006). Sheep fed on A. nummularia and S. virginicus simultaneously performed similarly than those on Rhodes grass. Abd El-Rahman (2003) recommended that mixing saltbush with wheat or barley straw results in significant increases in feed intake compared with either diet fed alone. He concluded also that feeding saltbush with low quality hay to sheep improves the use of the roughage and sometimes improved animal’s growth. 6. Conclusions This review summarized the benefits and the constraints of halophytes and other salt-tolerant plants as potential feed resources for sheep, goats and camels. It is concluded that: • Halophytes and salt-tolerant forages yield low to high edible biomass in saline lands where non-halophytic species cannot grow. • Many halophytes could be considered as potential sources of nitrogen and or major minerals for sheep and goats fed on low quality diets. However, energy supplementation of halophytes-containing diets is necessary to overcome nutrient requirements of animals. • Some anti-nutritive factors (ANFs) like lignin, oxalates and nitrates could restrict the utilization of some halophytes and salt-tolerant forages in livestock feeding mainly when they are used as sole diets. However, appropriate mixing of these species, based on their complementary roles, could dilute the negative effects of these ANFs, thus improves animal performances. • Although this review paper focused on studies carried out in Near East region, mainly in Egypt, it seems that a wide range of halophytes (Atriplex spp., Kochia spp., etc.) and salt-tolerant grasses (Sorghum, Sudan grass, etc.) could be considered as promising feed resources for small ruminants raised in saline lands and or in arid and semi-arid regions. The experience of other regions on the adaptation of these halophytes and other salt-tolerant plants to saline and or arid conditions and the success of their integration in feeding calendars which are described in the other papers of this special issue would strengthen the role of these alternative feed resources in the production systems of the saline agriculture. References Abd El Aziz, D.M., 1982. A study of the nutritive value of some range plants in the North Western Coastal Desert. Ph.D. Thesis, Faculty of Agriculture, Ain Shams University, Egypt. Abd El-Rahman, H.H., 1996. Utilization of desert range poor quality feeds by sheep and goats. M.Sc. Thesis. Faculty of Agriculture, Cairo University, Cairo, Egypt. Abd El-Rahman, H.H., 2003. Constraints and possibilities for their alleviation to improve utilization of desert natural range plants for grazing ruminants. Ph.D. Thesis, Faculty of Agriculture, Cairo University, Cairo, Egypt.

H.M. El Shaer / Small Ruminant Research 91 (2010) 3–12 Abd El-Rahman, H.H., 2008. Improvement of the nutritive value of some unpalatable desert plants by ensiling treatment with palatable plants and molasses additives. J. Agric. Sci. Mansoura Univ. 33, 8001– 8010. Anon., 2009. Introduction of salt-tolerant forage production systems to salt-affected lands in Sinai Peninsula in Egypt: a pilot demonstration project. Final Report, DRC, Egypt—ICBA, UAE. Anon. 2006. Electronic Conference on salinization: Extent of salinization and strategies for salt-affected land prevention and rehabilitation, 6 February–6 March 2006. Organized and coordinated by IPTRID (International Programme for Technology and Research in Irrigation and Drainage), FAO. Atiq-ur-Rehman, 1995. The potential for the use of saltbush (Atriplex spp.) in sheep grazing systems during summer and autumn in a Mediterranean environment. PhD Thesis. University of Western Australia, Perth. Atiq-ur-Rehman, 2002. Utilization of Atriplex as a forage under grazing and cut and carry systems for small ruminants. In: Proceedings of the International Symposium on Optimum Resources Utilization in Saltaffected Ecosystems in Arid and Semi-arid Regions, Cairo, Egypt, 8–11 April. Barry, T.N., McNabb, W.C., 1999. The implication of condensed tannins on the nutritive value of temperate forages fed to ruminants. Br. J. Nutr. 81, 263–272. Batanouny, K.H., 1996. Ecophysiology of halophyte and their traditional use in the Arab World. In: Choukr-Allah, R., Malcolm, C.V., Hamdy, A. (Eds.), Halophyte and Biosaline Agriculture. Marcel Dekker, Inc., USA, pp. 73–94. Bayoumi, M.T., El Shaer, H.M., Fawzia Assad, 1990. Survival of sheep and goats fed salt marsh plants. J. Arid Environ. 8, 75–78. Benjamin, R.W., Oren, W.E., Katz, E., Becker, K., 1992. The apparent digestibility of Atriplex barclayana and its effect on nitrogen balance in sheep. Anim. Prod. 54, 259–264. Ben Salem, H., Nefzaoui, A., Ben Salem, L., Tisserand, J.L., 1999. Different means of administering polyethylene glycol to sheep: effect on the nutritive value of Acacia cyanophylla Lindl. foliage. Anim. Sci. 68, 809–818. Burritt, E.A., Provenza, F.D., 2000. Role of toxin in intake of varied diets by sheep. J. Chem. Ecol. 26, 1991–2005. Davis, A.M., 1981. The oxalate, tannin, crude fiber and crude protein composition of young plants of some Atriplex species. J. Range Manage. 34, 329–331. El Shaer, H.M., 1981. A comparative nutrition study on sheep and goats grazing Southern Sinai desert range with supplements. Ph. D. Thesis, Faculty of Agriculture, Ain Shams University, Egypt. El Shaer, H.M., 1997. Sustainable utilization of halophytic plant species as livestock fodder in Egypt. In: Proceedings of the International Conference on “Water management, salinity and pollution control towards sustainable irrigation in the Mediterranean region”, September 22–26, 1997, Bari, Italy, pp. 171–184. El Shaer, H.M., 1999. Potentiality of animal production in the Egyptian desert region. In: Proceedings of the Conference on Animal Production in the 21st Century Challenges and Prospects, 18–20 April 2000, Sakha, Kafr El Sheikh, Egypt, pp. 93–105. El Shaer, H.M., 2004. Potentiality of halophytes as animal fodder under arid conditions of Egypt. Rangeland and Pasture Rehabilitation in Mediterranean Areas. Cahiers Options Méditerranéennes 62, 369–374. El Shaer, H.M., Kandil, H.M., 1990. Comparative study on the nutritional value of wild and cultivated Atriplex halimus by sheep and goat in Sinai. Comput. Sci. Dev. Res. 29, 81–90. El Shaer, H.M., Zahran, M.A., 2002. Utilization of halophytes in Egypt: an overview. In: Proceedings of the International Conference on “Halophyte Utilization and Regional Sustainable Development of Agriculture”, Huanghua, Shijiazhnag, China, 14–20 September 2001, pp. 20–26. El Shaer, H.M., Rammah, A., Nasr, A., Bayoumi, M.T., 1987. Nutritional quality of some grasses in North Sinai. In: Proceedings of the International Conference on Desert Development, January 25–30, 1987. Cairo, Egypt, pp. 15–19. El Shaer, H.M., Salem, O.A., Khamis, H.S., Shalaby, A.S., Farid, M.F.A., 1990. Nutritional comparison studies on goats and sheep fed broiler litter ensiled with desert shrubs in Sinai. In: Proceedings of the International Goat Production Symposium, October 22–26, 1990. Tallahassee, Fl, USA, pp. 70–74. El Shaer, H.M., Ali, F.T., Nadia, Y.S., Morcos, S., Emam, S.S., Essawy, A.M., 2005. Seasonal changes of some halophytic shrubs and the effect of processing treatments on their utilization by sheep under desert conditions of Egypt. Egyptian J. Nutr. Feeds 8, 417– 431.

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