Potential use of oldman saltbush (Atriplex nummularia Lindl.) in sheep and goat feeding

Small Ruminant Research 91 (2010) 13–28

Contents lists available at ScienceDirect

Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres

Review

Potential use of oldman saltbush (Atriplex nummularia Lindl.) in sheep and goat feeding夽 H. Ben Salem a,∗ , H.C. Norman b , A. Nefzaoui c , D.E. Mayberry b , K.L. Pearce d , D.K. Revell b a

Institut National de la Recherche Agronomique de Tunisie (INRAT), Laboratoire des Productions Animales et Fourragères, Rue Hédi Karray, 2049 Ariana, Tunisia b CSIRO Livestock Industries, Centre for Environment and Life Sciences, Private Bag 5, Wembley, WA 6913, Australia c ICARDA/North Africa Program, 1, rue des Oliviers, El Menzah V, 2037 Tunis, Tunisia d Division of Veterinary and Biomedical Science, Murdoch University, Murdoch, WA 6150, Australia

a r t i c l e

i n f o

Article history: Available online 25 February 2010 Keywords: Atriplex nummularia L. Fodder potential Sheep Goats

a b s t r a c t Overgrazing and mismanagement of rangelands, climate change, drought and ‘salinisation’ of lands are threatening the sustainability of production systems and the fertility of cropping lands worldwide. This alarming situation drew the attention of policy makers, scientists and technicians and motivated them to develop feasible and sustainable strategies targeting the promotion of livestock sector in arid and semi arid zones, drought mitigation, protection and better use of natural resources (i.e. rangelands and water sources) and combating soil and water salinity. There has been an increasing awareness of the value of shrubs in forage production and for rehabilitation of depleted rangelands. Among the wide range of multipurpose fodder trees and shrubs, oldman saltbush (Atriplex nummularia Lindl.) has received increasing interest as livestock forage and valuable revegetation species on marginal saline lands, especially in arid zones of Australia and in the West Asia and North Africa (WANA) region. Adapted to drought and water and soil salinity, oldman saltbush produces important consumable biomass in areas where other crops cannot grow. To cope with these harsh conditions, this species accumulates high levels of salt and oxalates on its leaves rendering them less palatable and decreasing their nutritive value. Even though, satisfactory performance of small ruminants fed on A. nummularia has been reported in numerous research studies. This paper presents a thorough review of the literature on fodder potential of oldman saltbush and highlights the main constraints and opportunities to make better use of this shrub for feeding sheep and goat under different production systems. © 2010 Elsevier B.V. All rights reserved.

1. Introduction Range vegetation used to be the main feed resource for livestock particularly in the arid and semi arid regions. In Tunisia, for example, the contribution of rangelands to

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. ∗ Corresponding author. Tel.: +216 71 230024; fax: +216 71 231592. E-mail address: [email protected] (H. Ben Salem). 0921-4488/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2009.10.017

ruminant feeding before the 1970s was around 80%. Currently this is less than 20% leading to an over-reliance on barley grain and concentrate feeds, and consequently to the fluctuating feeds availability and prices (Nefzaoui, 2002). For decades, rangelands in Africa, West and Central Asia suffered from overgrazing and many areas are severely degraded. Most flocks of sheep, goats and camels are raised in dry areas receiving less than 300 mm of rainfall. These areas are unsuitable for cultivation, but support native pasture characterised by low biomass and deficiency of necessary nutrients to grazing animals. Decreased vegetation cover is often accompanied with severe soil erosion,

14

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

especially wind erosion. The scarcity of range vegetation as opposed to increasing flock sizes generally results in mismanagement of native rangelands especially communally used ones. Because of this situation, planting of fodder shrubs would reduce or overcome feed shortage and erosion problems, in addition to their potential use in other domains (e.g. wood production, medicinal uses, etc.). Cultivated fodder shrubs are preferred to herbaceous species for rangeland revegetation. Livestock managers rely generally on the evergreen habit of shrub species as a source of nitrogen (e.g. Atriplex spp.), energy (e.g. cactus) and/or other nutrients. These shrubs provide also green forage for animals at times when grass and forbs are of low nutritional value, and provide a drought reserve when other forage sources are in short supply. But, the presence of plant secondary compounds (e.g. tannins, oxalates, saponins and alkaloids) could restrict nutrient utilisation of shrubby vegetation (Papanastasis et al. 2008). Even though, only few species, especially cactus and halophytes, can withstand the harsh edapho-climatic conditions in these areas (e.g. rainfall below 300 mm, high temperature, marginal soil, etc.). Soil and water salinity is another major constraint affecting dryland agriculture and animal production worldwide. Climate change, human activities (e.g. mismanagement of irrigation), reduced vegetation and a rising water table are contributing to a rapid expansion of saline soils worldwide. Ghassemi et al. (1995) estimated salinised soils at 14.8 Mha in Africa, 52.7 Mha in Asia and 0.9 Mha in Australia. About a decade later, the National Land and Water Resources Audit (2001) reported that saline land area in Australia reached 1.8 Mha and a further 6 Mha is at risk. Salinisation is progressing over many hectares of cropping soils and threatening the sustainability of production systems in numerous countries. The opportunities and limitations for animal production from saline land were well reviewed by Masters et al. (2007). Australian farmers have been successful in utilising and stabilising saline land through the establishment of halophytic shrub-based pastures for livestock production. The species most used to achieve these objectives are Atriplex spp., mainly oldman saltbush. Besides Australia, this salt-tolerant shrub is grown in the West Asia and North Africa (WANA) region (e.g. Egypt, Jordan, Libya, Morocco and Tunisia) and in southern Europe (e.g. Greece; Papanastasis et al., 2008) for livestock production across a range of rain fed and irrigated farming systems. The aim of this review paper is to develop a better understanding of the strengths and weaknesses of oldman saltbush for ruminant production and identify opportunities to improve the conversion of this halophyte species into animal products. 2. Geographical distribution and ecological characteristics Oldman saltbush occurs naturally in the semi arid and arid zone of southern and central Australia where it has evolved with predation by macopods such as kangaroos. The introduction of exotic shrub species in Tunisia began during the last years of the 20th century (Le Houérou and Pontanier, 1987). Between 1920 and 1930 oldman saltbush, A. semibaccata from Australia and A. canescens

from USA were introduced to Tunisia and Morocco. Further introductions took place in the whole region during the period from 1960s to 1980s under the framework of international research and development rangeland projects. Among about 400 species of Atriplex in the world, only 13 species and subspecies are used for rangeland rehabilitation and fodder production: A. halimus subsp. halimus, A. halimus subsp. schweinfurthii, A. mollis, A. glauca, A. leucoclada, A. nummularia, A. canescens subsp. canescens, A. canescens subsp. linearis, A. amnicola, A. undulata, A. repanda, A. semibaccata, and A. barclayana. The most important exotic species utilised on a large scale is A. nummularia (Tunisia, Morocco, Algeria, Libya, Egypt, Jordan, Syria and Spain) (Le Houérou, 1991). A. nummularia can develop under cultivation in the arid zone between the 200 and 400 mm isohyets of mean annual rainfall. Like other Atriplex species, oldman saltbush is able to reach water tables as deep as 10 m below ground surface. A single shrub can produce 1 kg of dry matter (DM) with only 250 kg of water. Arid zone saltbushes are considered the most heat-tolerant terrestrial dicotyledons. As in many plants with a C4 photosynthetic pathway, biomass growth of saltbush tends to be higher in summer and autumn where ambient temperatures are higher (Norman et al., 2009a). It can withstand minimum winter temperatures of −10 to −12 ◦ C for a few hours. It is well adapted to deep silty to silty-clay soils with low to moderate salinity (2–50 dS/m, Masters et al., 2007) under rainfall equal or above 200 mm. 3. Grazing systems using oldman saltbush The productivity of oldman saltbush grazing systems is determined by herbage production, both in terms of quantity grown and its time of production, interaction with understorey plants, voluntary feed intake and nutritive value. To achieve maximum profitability from oldman saltbush systems, animal production per unit of feed intake must be considered against direct costs (e.g. animal, establishment and/or maintenance costs) and indirect costs (e.g. environmental outcomes and opportunity costs). To survive, oldman saltbush requires recovery periods where it is rested from grazing and cannot support intensive and continuous grazing (Le Houérou, 1992). Under ideal conditions this shrub species should be exploited once a year during times of seasonal feed shortages during one to 2 months. In southeast Spain, Correal et al. (1990) concluded that oldman saltbush grazing should occur every 6 months in wet years and once a year in dry years. Oldman saltbush is very tolerant of saline conditions but has little tolerance to persistent waterlogging in the root zone (Barrett-Lennard, 2003). This is perhaps because it has deeper rooted than many Atriplex species, with roots descending more than 4 m (Barrett-Lennard, 2003). Oldman saltbush is used in several types of saline production systems including; saline groundwater with non-saline, highly transmissive, permeable soils (as in parts of the Eastern Mediterranean), highly saline groundwater with saline and/or sodic soils (as in large parts of Central Asia and Australia) and saline irrigation or drainage waters (in the USA) (Ghassemi et al., 1995 from Masters et al., 2007). Oldman saltbush is also used for forage production in non-saline

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

15

Table 1 Productivity of oldman saltbush across a range of farming systems. Country

Location

EDM* (t/ha)

Plants/ha

EDM/shrub (kg/yr)

Conditions

Argentinaa Australiab Australiac Iraqd Israele Israele Tunisiaf USAg

Mendoza Lake Grace Yealering Dalmaj Negev Negev Saouef Arizonia

3.3 0.7 0.5 2.52 0.9 3.2 3.5 12.3

4665 650 670 400 625 10000 2500 17000

0.7 1.1 0.7 6.3 1.4 0.3 1.4 0.7

Mildly saline water table (1 m) Rain fed (350 mm) and highly saline water table Rain fed (362 mm) Rain fed (80 mm) and irrigation (18.2 mm) Rain fed (227 mm) Rain fed (227 mm) Rain fed (390 mm) Irrigated

a b c d e f g *

Guevara et al. (2008). Norman et al. (2009a,b,c). Norman et al. (2008). Abdul-Halim et al. (1990). Benjamin et al. (1995). Ben Salem et al. (2005a). Watson et al. (1987). EDM, edible dry matter.

low rainfall systems (Benjamin et al., 1995; Guevara et al., 2008). Oldman saltbush forage tends to be used as a drought reserve or to fill annual feed shortages within grazing systems on agricultural (rather than range) land (Le Houérou, 1991). For example oldman saltbush is used to fill the summer/autumn feed gap typical of Mediterranean-type climates in Syria (Osman et al., 2006), southern Europe (Papanastasis et al., 2008) and Australia (Morcombe et al., 1996), and to fill an early winter feed shortage in the Mendoza plain area of Argentina (Guevara et al., 2008). In other systems oldman saltbush is integrated into the diets of animals throughout the year, for example in Jordan (AbuZanat et al., 2003) and Tunisia (Ben Salem et al., 2005a). A recent study by Wilmot and Norman (2006) suggests that oldman saltbush may not be utilised most efficiently as a ‘living haystack’ to be used only as a drought reserve unless the plants are managed with annual grazing. They found that plants that were not heavily grazed for a short period of time at least once per year, tended to drop leaves and not grow as fast as grazed plants. After 3 years of management by heavy annual grazing (in autumn) there was the same amount of biomass by the following summer as there was on ungrazed oldman saltbush plants. 4. Biomass production and growth There is considerable variation in reported ‘edible’ dry matter (EDM) production from oldman saltbush. Table 1 presents EDM production ranging from as little as 0.5 t/ha/yr in a saline paddock in southern Australia (Norman et al., 2008) to 12 t DM/ha/yr under irrigation in Arizona (Watson et al., 1987) and 15–20 t/ha/yr in Libya and Tunisia (Le Houérou and Pontanier, 1987). According to the latter authors, irrigated with saline water, oldman saltbush produced more than 5 t DM/ha/yr. While these are large differences in productivity when expressed as EDM/ha, individual shrubs tend to typically produce around 1 kg EDM/yr, with a few exceptions. Hence the large reported differences in productivity across production systems are largely associated with planting density, although there is evidence of declining yield per shrub as planting density increases (Benjamin et al., 1995). Variation in the produc-

tivity of oldman saltbush plantations is also function of a range of factors including water availability, level of soil and water salinity (Barrett-Lennard, 2003), waterlogging, soil texture (Barrett-Lennard, 2003), soil fertility (AbuZanat et al., 2004), colonisation of the roots by mycorrhyzal fungi (Plenchette and Duponnosis, 2005) and plant genotype (H. Norman, unpublished data). It is worthy to note that oldman saltbush, in contrast to many other woody species, has the capacity of producing buds and twigs on the stem and the main branches. After defoliation, oldman saltbush does not need continued cutting to maintain its productivity of EDM (Benjamin et al., 1990). The lifespan of a well maintained and managed oldman saltbush plantation could reach up to 40 years (Le Houérou, 1965). Depending on grazing intensity, oldman saltbush plantation could be pruned at 4–6 year intervals (Le Houérou, 1992). It can be difficult to compare EDM between studies due to variation in definition of the ‘edible’ component. While all authors agree that EDM comprises of leaves and soft twigs, the acceptable diameter of twigs varies from less than 6 mm (Van der Baan et al., 2004) to less than 3 mm (Norman et al., 2004, 2008) and as little as less than 1.5 mm (Franklin-McEvoy et al., 2007). While all these classifications are valid, in that if animals are pushed far enough they will eat twigs of increasing diameter, it makes comparisons of biomass production and nutritive value problematic. Ben Salem et al. (2005a) found that EDM represents 27–40% of the biomass of whole, mature plants while Le Houérou (1986) found it was about 50%. While this review focuses on biomass for livestock production, the woody component of the shrubs may be a valuable fuel resource (Qureshi and Barrett-Lennard, 1998). Oldman saltbush has a C4 photosynthetic pathway and biomass growth tends to be higher during the warmer months if other resources are not limiting. Fig. 1 presents some growth rate data from a large oldman saltbush plantation in Lake Grace, Western Australia. The research site consisted of 10 plots of oldman saltbush shrubs subject to a range of grazing regimes and has a Mediterraneantype climate with 350 mm annual rainfall. The shrubs grew almost 6 g of EDM/day in the hot, dry autumn months and only 1 g EDM/day during spring, when temperatures

11.4 (ME)

6.3 (ME)

1.1 3.0

1.5 28.5 17.7 22.5 22.4 28.9

15.2 15.5 34.8

33.2 44.7 33.6 44.5 40.9 45.5

17.1 27.5 37.9 40.7

8.0

13.7 9.8 14.5 10.2 6.4 9.0

2.57 (NE) 2.59 (NE) 3.1 2.3 10.3

8.1 17.1 24.6 30.5 38.8

8.5

ADF

28.2 21.6

10.4 13.8

7.5 9.7

8.4 26.9

Nutrient contents of oldman saltbush differ among studies (Table 2) and varied in general between leaves and twigs. Overall these edible parts are relatively high in ash and crude protein but low in energy. The variation of the concentrations of these nutrients and their availability is discussed below.

20.6 15.4 13.4 12.4 18.9 17.5 12.8 17.2 14.6 13.7 25.2 22.9 23.4 17.0 19.7 17.8 18.6 10.3 23.6 24.0 25.5 29.4 23.0

5.1. Nitrogen value

*

**

L, leaves; LT, leaves and twigs; NI, not indicated. ME, metabolisable energy; NE, net energy.

28.5 28.6

15.3

29.5 28.3

31.4 37.0 25.0

24.2 28.0 17.9 35.4 25.0 34.4 25.2 21.6 21.4 30.8 24.3 19.8

L LT NI L LT LT LT LT L LT L LT L LT LT LT NI LT Australia Australia Australia Chili Egypt Ethiopia Jordan Libya Libya Morocco Saudi Arabia South Africa South Africa Spain Tunisia Tunisia USA USA

Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed NI Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Irrigated with saline water Irrigated

Ash DM (%)

were cooler. The cost of carrying livestock through periods of feed scarcity is a major limitation to many extensive animal production systems, and the growth patterns of oldman saltbush complement annual plant systems in Mediterranean-type climates, where the annuals are dead and of poor nutritive value during the hottest months (Papanastasis et al., 2008). 5. Nutrients in oldman saltbush foliage

Plant parts*

Rain-fed or irrigated

Fig. 1. Daily growth (g edible dry matter/shrub) of old man saltbush across two seasons at a saline site in Lake Grace, Australia. Saltbushes were measured in 5 transects within 10 plots, each at different stages of recovery from grazing. The site has a Mediterranean-type climate and annual rainfall averages 350 mm, the majority falling in winter and spring. There was a highly saline water table (7500 mS/m) within reach of the OMSB roots (see Norman et al., 2009a).

Country

Table 2 Nutrient contents of oldman saltbush (% DM, unless otherwise indicated).

Crude protein

Crude fibre

NDF

ADL

Ether extract

7.9 (ME)

Energy** MJ/kg DM

Wilson (1977) Norman et al. (2004) Kumara Mahipala et al. (2009) Hirsch-Reinshagen et al. (1986) Hassan and Abdel-Aziz (1979) Kaitho et al. (1998) Abu-Zanat and Tabbaa (2006) Le Houérou et al. (1982) Le Houérou et al. (1982) Chriyaa and Boulanouar (2000) Khalil et al. (1986) De Kock (1980) Van Niekerk et al. (2004a) Silva-Colomer et al. (1986) Saadani et al. (1989) Ben Salem et al. (2004) Watson (1990) Watson and O’Leary (1993)

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

References

16

The crude protein (CP) content of oldman saltbush EDM ranges between 10 and 25% DM. This wide variation is likely due to the different edapho-climatic conditions, age of plants and seasons. Under rain-fed conditions (400 mm/yr) in a semi arid area (Saouef, Tunisia), the EDM of a 15yr-old oldman saltbush plantation had the highest CP content in spring and lowest in summer (Ben Salem, 1998). Except in few studies (see Table 2), the CP content is usually above 15% DM. This characteristic is, a priori, interesting for dry areas where herbaceous vegetation is scarce. However, much of oldman saltbush nitrogen is associated with non-protein compounds such as nitrates, glycinebetaine and proline. Glycinebetaine and proline are concentrated in oldman saltbush leaves and help the plant cope with hydrolic and saline stresses (Le Houérou, 1992). The glycinebetaine (N,N,N-trimethyl glycine) is degraded by rumen microflora when adequate quantity of energy is available and can enhance the utilisation and digestion of salty feed by microorganisms and the host animal (Le Houérou, 1992). Ben Salem et al. (2002c) found that about 65% of total nitrogen in oldman saltbush EDM is soluble.

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

17

Table 3 Amino acid composition (g/16 g N) of oldman saltbush foliage. Amino acids Aspartic acid Threonine Serine Glutamic acid Proline Glycine Alanine Valine Methionine (M) Cystine (C) M+C Isoleucine Leucine Tyrosine (T) Phenylalanine (P) T+P Lysine Histidine Arginine Tryptophan NH3 CP (% DM)

Wehren (1976) 7.10 3.26 3.31 8.12 3.80 4.09 4.54 4.54 1.42 1.84 3.26 3.70 5.98 2.63 3.84 6.47 4.73 1.71 4.40 7.23 21.4

Khalil et al. (1986) 5.96 2.90 3.12 6.89 3.22 3.54 3.79 3.65 0.87 0.69 1.56 3.27 5.04 1.99 3.20 5.19 5.44 1.53 5.30 0.62 2.53 25.2

Non-protein compounds may be converted into microbial protein in the rumen, but the extent to which this occurs depends on the availability of metabolisable energy (ME), which is low in the EDM of oldman saltbush. With insufficient energy, these compounds are converted to ammonia in the rumen, which is absorbed by the animal, converted to urea and excreted in the urine. Despite this potential loss of nitrogen, Abou El Nasr et al. (1996) found that sheep fed fresh oldman saltbush only had positive nitrogen balance and achieved approximately 150% of their maintenance requirement. The amino acid composition of oldman saltbush EDM (Table 3) does not indicate any deficiencies. In particular, the essential amino acids, methionine and lysine are higher than in cereal proteins and are close to the level of the FAO/WHO reference protein score (Khalil et al., 1986). 5.2. Minerals The mineral concentrations of oldman saltbush present a range of positive and negative scenarios, depending on the minerals accumulated within the oldman saltbush foliage and the mineral and physiological status of the animals. Most of the salt in oldman saltbush is sodium chloride and potassium chloride; however oldman saltbush also contains high concentrations of S, Mg, Ca and P (Table 4). While most of these minerals are present in concentrations above the recommended daily intake for ruminants (Standing Committee on Agriculture, 1990), the complex interactions between minerals means that livestock grazing saltbush alone may be predisposed to mineral imbalances (Masters et al., 2007). Mayberry et al. (unpublished data) indicate that sheep grazing oldman saltbush for an extended period of time without supplementation could develop Mg, Ca and P deficiencies. These three minerals are stored in bone, and can be mobilised when dietary intake and absorption is inadequate (Underwood and Suttle, 1999). Combined, Mg,

Silva and Pereira (1976) 5.10

FAO/WHO (1973) 4.00

5.00 1.90

5.40 9.60

3.50 4.00 7.00

5.20 5.50

6.00 5.50

1.00 20.1

Ca and P deficiencies can cause loss of appetite, stunted growth, bone deformitites, reduced lamb survival, hypomagnesaemic tetany (grass tetany) and hypocalcaemia (milk fever) (Standing Committee on Agriculture, 1990). The effects on animal production and the likelihood of stock deaths are exacerbated when multiple deficiencies occur simultaneously. Franklin-McEvoy and Jolly (2006) took blood samples from dry (non-pregnant) sheep on four properties in the central north-east pastoral zone of South Australia. The sheep had access to a variety of chenopodic shrubs, including oldman saltbush and Atriplex vescaria, Maireana brevifolia and Rhagodia spp. Sheep on all properties had blood Ca concentrations below the recommended daily minimum of 2.9 mmol/L, despite consuming adequate levels of Ca in the diet. Blood Mg and P concentrations were at the low end of the recommended range, and K was high. Aazzeh and Abu-Zanat (2004) also found that feeding saltbush (oldman saltbush, and A. halimus plus a concentrate ration) to lactating ewes led to a net loss of Ca, but an increase in the blood serum concentrations of P. Calcium, Mg and P deficiencies are likely to be due to a combination of reduced availability and absorption of minerals from oldman saltbush leaves. Some minerals are more resistant to removal from plant material than others, with P being the most resistant, followed by Ca, Na, Mg and K (Playne et al., 1978). High water intakes by sheep eating saltbush can flush feed particles from the rumen before minerals can be released, and remove minerals from the rumen before they can be absorbed. More specifically, high K concentrations interfere with Mg absorption from the rumen and the rest of the gastrointestinal tract (Newton et al., 1972; Dalley et al., 1997). Oxalates can bind to Ca to form Ca-oxalates, which are insoluble and not readily metabolised by ruminal microorganims (McDowell, 1992; Underwood and Suttle, 1999). In addition, the dietary cation-anion different (DCAD) of oldman saltbush is high, which would be unfavourable for promoting Ca mobilisa-

0.4

285.1 391 9.3

0.45 0.43 11.76

7.17 2.03 0.46 0.20 0.55 LT USA

L, leaves; LT, leaves and twigs; NI, not indicated.

2.89

LT NI LT LT L NI L L LT LT NI Australia Australia Egypt Libya Libya Morocco Saudi Arabia South Africa Tunisia USA USA

*

4.70

3.95 3.06 3.20 2.49

0.07 0.04 0.20 0.24 0.16 0.18 0.68 0.68 1.30 1.44 1.09 1.36

0.76 0.30 0.84

7.25 4.80 7.77 3.95 6.30 4.20 4.85 0.15 0.25 0.77 0.69

0.77 0.65

3.63 1.9

12.9 12.3 7.90 6.30 3.0 5.6 0.14 0.17 L L L Australia Australia Australia

Rain fed Irrigated with saline water Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Rain fed Irrigated with saline water Irrigated

0.60 0.30

Watson and O’Leary (1993)

13.0 5

74 62 56.5 44 54 14 47.0 30 420

3.5 18.84 24.0 189.5 101.5

24

146.68 50.8

Mn (mg/kg DM) Cu (mg/kg DM) Zn (mg/kg DM) Ca P Mg K Na Cl S Fe (% DM) (% DM) (% DM) (% DM) (% DM) (% DM) (% DM) (mg/kg DM) Plant parts*

Rain-fed or irrigated

5.3. Fibre and energy

Country

Table 4 Mineral contents of oldman saltbush.

tion. The DCAD value of oldman saltbush varies depending on the equation used, but for a large number of samples collected in Western Australia, it is typically in the range of 60–90 mEq/100 g (D.K. Revell & H.C. Norman, unpublished data). In addition to these deficiencies, sheep grazing saltbush alone could also suffer sulphide toxicity. Diets containing 2.5–3.5 g/kg DM of S are deemed to be high for sheep (Standing Committee on Agriculture, 1990), and Norman et al. (2004) has measured S levels in oldman saltbush of 4.8 g/kg DM. If S is not incorporated into microbial protein in the rumen, the resulting high sulphide levels can reduce voluntary feed intake, reduce rumen motility, cause damage to the central nervous system and reduce Copper (Cu) absorption (Bird, 1972; Underwood and Suttle, 1999). Cu deficiencies are also a problem, causing loss of wool pigmentation (steely wool), decreased growth rate, bone fragility, diarrhoea and anaemia (Standing Committee on Agriculture, 1990). However, when combined with an annual pasture system, saltbush may provide a valuable source of S to livestock at risk of S deficiencies. Boron (B) concentrations of oldman saltbush ranged from 106 to 189 mg/kg (Watson et al., 1994). This trace mineral apparently has an essential function that regulates parathyroid hormone action, and therefore, indirectly influences metabolism of Ca, P, Mg, and cholecalciferol (McDowell, 2003). To our knowledge there are no data on toxicity level of boron for sheep and goats. However, cows consuming 150 or 300 mg B/L of water exhibited inflammation and oedema in the legs and around the dew claws, and reduced feed intake, growth, hematocrit, haemoglobin, and plasma P (see McDowell, 2003). Therefore, sheep or goats consuming more than one kg DM of oldman saltbush could show toxicological signs.

0.60 1.39

Norman et al. (2004) Kumara Mahipala et al. (2009) Hassan and Abdel-Aziz (1979) Le Houérou et al. (1982) Le Houérou et al. (1982) Sarson and Salman (1977) Khalil et al. (1986) Van Niekerk et al. (2004b) Ben Salem et al. (2004) Watson et al. (1994) Watson (1990)

Se (mg/kg DM)

Wilson (1977) Beadle et al. (1957) Beadle et al. (1957)

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

Reference

18

Fibre content of oldman saltbush foliage is in the range of that reported in other fodder shrubs (Table 2). Cell wall (NDF) level varied between 30 and 45% DM and the lignocellulose fraction (ADF) ranged between 15 and 29% DM. The ADL fraction ranged between 6 and 14% DM, which is similar to levels found in the foliage of many other woody species. Because of its high ash content, the ME content of oldman saltbush DM is low relative to that of herbaceous species. The few in vivo digestibility studies of oldman saltbush suggest that it provides only low to moderate energy to sheep. While reported levels of in vivo organic matter digestibility (OMD) appear to be high (see Table 6), the high levels of soluble salts in the plants mean that there is a low digestible organic matter in the dry matter (DOMD) so that animals still need to consume high levels of DM to meet their energy requirement (Masters et al., 2005a,b; Norman et al., 2009b). As discussed previously, these levels of salt can limit voluntary feed intake (VFI) so animals may not be able to eat enough energy to maintain weight. Further, high salt incurs a metabolic energy cost to process and can lower the efficiency of digestible energy to ME by up to 10% (Arieli et al., 1989; Masters et al., 2005a,b). Based on data reported in Table 2, the average ratio of digestible CP (g/kg

1.4d

Saponins % DM

c

d

b

Nd 4.2

L, leaves; LT, leaves and twigs; S1, stem tips of young plant; S2, stem tips of mature plant; NI, not indicated. Expressed as tannic acid equivalent. Expressed as equivalent gallotannic acid. Expressed as leucocyanidin equivalent. Expressed as g equivalent diosgenin/kg DM. *

a

< 1a

2.9c

0.2 0.5 0.2 1.2a 2.0a 1.2a

1.4 2.4 1.5 1.1 ± 0.3 0.3 L S1 S2

Australia Australia Australia Australia Jordan Jordan Jordan Tunisia Tunisia Tunisia Tunisia USA USA USA

LT LT LT LT LT LT LT NI (12 wk-old) NI (22 wk-old) NI (30 wk-old)

4.5–6.4b 3.6–8.8b

1.0 1.6 1.1 0.6 ± 0.04c < 1c

Condensed tannins % DM Total tannins % DM Total phenols % DMa Plant parts* Country

Table 5 Secondary compounds in oldman saltbush.

6. Anti-nutritive factors in oldman saltbush foliage

7.0 ± 1.1 3.7 7.0 7.3 9.1 4.2 2.8

5.8 4.7–8.8 1.3–2.1 3.29

Hydrolysable tannins % DM

Total oxalates % DM

Data on vitamins in shrub foliage are scarce. Vitamin A is of most importance to range ruminants because it is most likely to be deficient. It is needed to prevent night blindness, eye lesions, general degeneration of the nervous system, and unsuccessful reproduction. Beta carotene is the major source of vitamin A in shrubs and in some areas they are a valuable source of vitamin A for animals grazing on winter ranges. According to Aguer (1973) and Ben Ameur and Blomeyer (1974), the carotene content of oldman saltbush EDM was 41.0 and 34.5 mg/kg DM, respectively. Oldman saltbush appears to be a valuable source of vitamin E. Pearce et al. (2005) found that oldman saltbush has high concentrations of the antioxidant vitamin E (or the tissue active form of this vitamin; ␣-tocopherol at 139 mg/kg EDM). White and Rewell (2007) found that 58% of weaner sheep flocks in the Mediterranean-type climate areas of Australia had vitamin E deficiency when sampled in autumn, with 6% showing symptoms of severe muscle damage. The strategic use of oldman saltbush could help address this problem.

3.1 4.5

Soluble oxalates % DM

5.4. Antioxidants

Almost all woody species contain secondary compounds in their foliage, seeds, fruits and or roots (Makkar et al., 2007). The most common secondary compounds in shrub foliage include tannins, oxalates, saponins and alkaloids. Depending on their level in the diet, structure and activity, each of these secondary compounds could reduce feed intake, disturb microflora activity, and influence the productive and reproductive performances of livestock. In extreme cases they can kill an animal. However, the consumption of low amounts of tannins and saponins could have positive effect on the animal performances through, for example, in situ protection of dietary proteins from rumen degradation, defaunation effect, a decrease of methane production, improved nutrient utilisation, etc. The contents of total phenols, condensed tannins and

0.25

Nitrate (g/kg DM)

References

DM) to ME (MJ/kg DM) is 16. For maintenance requirements of sheep a digestible CP (2.52 g/kg BW0.75 ) to energy (0.4 MJ ME/kg BW0.75 ) ratio of 6 is required (INRA, 1978) indicating that the energy concentration in oldman saltbush could be a limiting factor, especially when the level of readily available energy is also low in dry herbage diets that may typically be on offer with saltbush (Wilson, 1977; Hassan and Abdel-Aziz, 1979). The gap of ME has to be supplied from another feed resource if available (e.g. barley). Digestible OM values of oldman saltbush range from 460 to 540 g/kg OM (adapted from Wilson, 1966; Hassan and Abdel-Aziz, 1979; Watson et al., 1994; Ben Salem, 1998) and sheep lose large amounts of energy in the faeces and as methane (Arieli et al., 1989; Mayberry et al., 2009). These energy losses are greater than can be explained by salt alone and could be associated with secondary compounds. A number of grazing studies have demonstrated that sheep cannot maintain liveweight on saltbush alone (Wilson, 1966; Warren and Casson, 1992; Ben Salem et al., 2005a).

19

Wilson (1966) David (1981) David (1981)) Norman et al. (2004) Abu-Zanat et al. (2003) Abu-Zanat et al. (2003) Abu-Zanat et al. (2003) Ben Salem (1998) Ben Salem et al. (2002c) Ben Salem et al. (2002a) Ben Salem (unpublished) Watson et al. (1987) Watson et al. (1987) Watson et al. (1987)

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

20

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

hydrolysable tannins in oldman saltbush foliage (Table 5) appear low enough to avoid negative effects on grazing or stall-fed ruminants. Plants growing in saline soil, like oldman saltbush, need oxalates for osmo-regulation of Na, K and Cl ions (Cymbaluk et al., 1986). Plants containing 10% oxalate or more are considered toxic and should not be grazed (James, 1977). Allison et al. (1977) reported that sheep ingesting between 39 and 51 g of calcium oxalate per day are likely to develop acute signs of toxicity. However, sheep have eaten 6% oxalate without signs of toxicity (James and Butcher, 1972). Theoretically, if sheep consume oldman saltbush alone, they will ingest about 132 g of calcium oxalate (6.6% calcium oxalate = 66 g per kg DM × 2 kg per day per sheep = 132 g) and are likely to develop signs of toxicity. Oxalates can be toxic to ruminants, through the formation of calcium oxalate crystals in blood capillaries leading to cellular damage (James and Butcher, 1972). Formation of a complex with calcium leads to a decrease in availability and this can lead to hypocalcaemia, osteoporosis, rumen stasis and gastroenteritis (Standing Committee on Agriculture, 1990; Abu-Zanat et al., 2003; Masters et al., 2009). Practically however, the potential of toxicoses due to oxalate levels present in the browse of saltbush is low because of selectivity, impact of oxalates on voluntary feed intake and adaptation of ruminants to high levels of oxalate. Additionally, high salt may limit intake before oxalate toxicity is reached. Sheep are able to detect oxalates in feed and adjust VFI. Burritt and Provenza (2000) found that lambs offered a diet containing 3% oxalate ate half the amount of DM as lambs offered a control diet. While Norman et al. (2004) did not detect a relationship between oxalate concentrations and relative palatability, the oldman saltbush in the study had mean oxalate levels of only 3.1%. Other authors have reported much higher levels of oxalate including 7.6–9.6% (Abu-Zanat et al., 2003), 5.8% (Wilson, 1966) and 2–8% (David, 1981). Oxalate levels decline as oldman saltbush plants mature (David, 1981; Abu-Zanat et al., 2003) and vary according to season and edaphic environment (Abu-Zanat et al., 2003).

and the need for a large quantity of drinking water (up to 10.5 mL/g DM per day). It might not be practicable to provide this much water under farm conditions. VFI of oldman saltbush is limited by salt accumulation. Sheep stop eating salty forage after they have ingested approximately 200 g of salt in a day (Masters et al., 2005a,b). The concentration of salt in saltbush ranges from 154 to 350 g/kg EDM (Beadle et al., 1957; Watson et al., 1987), although values greater than 250 g/kg DM are more commonly reported. A 50 kg mature whether feeding on oldman saltbush with an ash concentration of 250 g/kg EDM and a digestibility of 50% will stop eating after ingesting about 800 g of herbage DM, which is 250 g less than that required to maintain live weight (Freer et al., 1997; Masters et al., 2009). Salt is a physiological limitation to intake in that animals can only eat salty forage as fast as they can excrete salt so long term adaptation to salt is unlikely (Masters et al., 2005a,b). Table 6 summarises some of the feeding trials with oldman saltbush. Overall, oldman saltbush VFI by sheep ranges from 16 to 119 g DM/kg BW0.75 while that by goats varied between 45 and 54 g DM/kg BW0.75 . Factors other than salt are likely to influence VFI of oldman saltbush. An experiment by Norman et al. (2004) demonstrated considerable variation in palatability between individual oldman saltbush plants that was not associated with salt, suggesting the possibility that secondary plant compounds could also influence diet selection and VFI. The high levels of sulphur in oldman saltbush could limit VFI (Norman et al., 2004; Norman et al., 2008). Recently, Norman et al. (2009c) investigated the potential of using carbon isotopes in faeces, blood plasma, rumen contents or wool to predict the relative intake of old man saltbush (with a C4 photosynthetic pathway) and other plant species (with a C3 photosynthetic pathway) in the diet of ruminants. For faecal samples, the organic matter content of the diet originating from saltbush could be predicted with a mean error as low as 2.7%. This technique provides a valuable tool for researchers as an understanding of what animals select allows for development of appropriate grazing management strategies to optimise productivity and/or persistence of target species.

7. Animal response to oldman saltbush feeding 7.2. Water intake The nutritive value refers to the responses in animal production per unit of voluntary feed intake and is a function of digestibility of nutrients and the efficiency with which the nutrients are used. 7.1. Voluntary feed intake Variation in VFI accounts for at least 50% of the variation that is observed in feeding value of forages (Ulyatt, 1973). Decreases in food intake result from the interactions between taste and postingestive feedback (Provenza, 1995, 1996). Palatability therefore is the interrelationship between flavour (odour, taste and texture) and postingestive feedback from nutrients and toxins which depends on the animals prior grazing experiences (Burritt and Provenza, 2000). The VFI of sheep on pure oldman saltbush diets is variable and ranges from 37 to 115 g DM/kg BW0.75 (Table 6). This is probably the result of the high salt content

The main constraint of the wide adoption of oldman saltbush plantation by farmers in the dry areas is the need for high amounts of drinking water to excrete the ingested salt. Where drinking water is freely available this may be of no concern, but where the supply is limited, as is often the case in the WANA region and Africa, it may be a serious limitation to the use of oldman saltbush as an animal food. Based on Table 6, the amount of drinking water consumed by sheep and goats fed on oldman saltbush alone or associated with feed supplements varied between 0.5 and 7 L/day. The amount of water drunk by sheep and goats is particularly high when oldman saltbush is fed alone, but it decreases when feed supplements are offered. Correal et al. (1992) noted a seasonal variation of the need of ewes for water when fed on oldman saltbush. The ewes consumed 6–8 L/day in autumn and 7–10 L/day in summer. Wilson (1974) reported a higher amount of water (12 L/day) con-

Table 6a Intake, digestibility, nitrogen balance and growth of penned sheep and goats fed on oldman saltbush-based diets. Country

Animal (breed)

Intake (g DM/day)

(days)

Atriplex

Supplement

749 720

None None

432 715

None None

681

None

695

Cut and carry use of oldman saltbush Australia Ewes (Merino) 21 Australia Wethers 28 (Merino) Australia Wethers 35 Australia Wethers (Merino) Egypt Rams (Barki x 14 Merino) 10 Egypt Rams (Barki x Merino) Egypt Rams (Barki x 10 Merino) Egypt Rams 7 Egypt Rams 7 Egypt Bucks 7 Egypt Bucks 7 Libya Ewes 231 Libya Ewes 238 (Barbarine) 105 Libya Lambs (Barbarine) Spain Spain Spain Tunisia Tunisia

Goats (Granadina) Ewes (Segurena) Ewes (Segurena) Lambs (Barbarine) Lambs (Barbarine)

Water intake (l/day)

DMD (%)

OMD (%)

CPD (%)

NDFD (%)

CFD (%)

N balance (g/day)

LW (kg)

Growth (g/day)

References

74.0

67.0

83.0

45

−57

a b

68.8 47.6

82.0

61.1

78.8

78.2

None

72.1

66.8

46.2

−4.1

49.3

−80

f

835

129, Barley

74.6

73.3

50.0

+ 6.2

45.8

+ 63

f

756 651 600 513 2050 2000

150, Barley None 150, Barley None 400, Barley None

56.6 48.2 57.2 49.3

60.2 63.2 63.2 66.3

<0 <0 <0

33.5 34.5 25.0 26.0 44.7 45

+ 56 −11 + 4.9 −9 + 10 +9

g g g g h i

240

+ 101

j

5.6

61.7

4.7 6.7 3.1 3.9

60.1 58.4 61.0 58.0

70.4 −10 42.8

c d e

72

320

Grazing (8 h/day) + 130, Cactus 320, ABS*

65

1520

None

6.5

(+ 4.9%)

l

65

1120

700, Straw

6.2

(+10.8%)

l

20

304

258, Barley

2.7

72.1

77.1

80.8

7.7

23.1

+ 66.7

m

20

150

288, Cactus

0.5

66.6

78.1

71.0

2.1

20.1

+ 20.5

m

57.4

50.4

77.5

45.2

0.7

k

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

Duration

*ABS, alfalfa + barley + sunflower. a, Wilson (1966); b, Weston et al. (1970); c, Wilson (1977); d, Mayberry et al. (2009); e, Hassan et al. (1979); f, Hassan and Abdel-Aziz (1979); g, Kandil and El Shaer (1989); h, Dumancic et al. (1982); i, Le Houérou (1991); j, Le Houérou (1992); k, Silva-Colomer et al. (1986); l, Correal and Stomayor (2000); m, Ben Salem et al. (2005a). DMD, dry matter digestibility; OMD, organic matter digestibility; CPD, crude protein digestibility; NDFD, neutral detergent fibre digestibility; CFD, crude fibre digestibility; N, nitrogen; LW, live weight.

21

22

Table 6b Intake, digestibility, nitrogen balance and growth of penned or grazing sheep and goats fed on oldman saltbush-based diets. Country

Animal (breed)

Intake (g DM/day)

Water intake

DMD

OMD

CPD

NDFD

CFD

N balance

LW

Growth

Atriplex

Supplement

(g/day)

(%)

(%)

(%)

(%)

(%)

(g/day)

(kg)

(g/day)

527 597 864 356 378 100

360, Barley 314, Barley None 500, Cactus + 207, Straw 399, Straw + 168, Barley Rangeland + 100, cactus

25

+108

61.6 52.5 72.1 68.1

60.5 47.9 75.4 68.2

76.0 72.6 72.8 71.3

40.4 31.6 73.5 68.2

19.5 19.5

+81 +59 +60

n n n o o p

710 1140

None 400, Barley + herbage ad lib. None 350, Barley 1000, Straw None 350, Barley 1000, Straw None 350, Barley 1000, Straw None 360, Barley 300, Cactus

+82 +34 +34 +67 +51 +53 +101 +61 +56 +70 +65 −35 +67 +20

q r s s s s s s s s s t t t

Tunisia Lambs (Barbarine) 90 Tunisia Lambs (Barbarine) 30 Tunisia Lambs (Barbarine) 30 Tunisia Lambs (Barbarine) 60 Tunisia Lambs (Barbarine) 60 Tunisia Kids (Boer) 92 Free grazing of oldman saltbush plantations Australia Ewes (Merino) Libya Ewes 231 Morocco Ewes (Timahdite) 90 Morocco Ewes (Timahdite) 90 Morocco Ewes (Timahdite) 90 Morocco Rams (Timahdite) 90 Morocco Rams (Timahdite) 90 Morocco Rams (Timahdite) 90 Morocco Wethers (Timadite) 90 Morocco Wethers (Timadite) 90 Morocco Wethers (Timadite) 90 Tunisia Lambs (Barbarine) 77 Tunisia Lambs (Barbarine) 77 Tunisia Lambs (Barbarine) 77

12.7 6.6 12.2 7.5

n, Ben Salem (1998); o, Ben Salem et al. (2004); p, Ben Salem et al. (2000); q, Norman et al. (2004); r, Dumancic et al. (1982); s, Tazi et al. (2000); t, Ben Salem et al. (2005a).

42.7

References H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

Duration (days)

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

sumed by sheep fed on oldman saltbush. It is clear that water consumption by sheep and goats fed on oldman saltbush-based diets would depend on the type and level of associated feeds and the ambient temperature. The low digestibility of oldman saltbush could be partly due to the high amount of water consumed by sheep or goats. This would result on decreased adhesion of bacteria to feed particles in the rumen and in an increased turnover rate of solid and liquid phases in the rumen. While watering sources in the dry areas are scarce with moderate to high content of salt, the combination of oldman saltbush and succulent species could be a promising solution. The complementary roles of oldman saltbush foliage and cactus cladodes were reviewed by Nefzaoui (2002). Cactus is a succulent drought tolerant range species. It is characterised by higher water use efficiency as compared to oldman saltbush (De Kock, 1980). Cactus cladodes are extremely low in DM (50–100 g/kg fresh material), nitrogen and fibre but high in sugars. Therefore, in addition to nutrient provision, sheep or goats receiving the mixture of oldman saltbush and cactus would need less drinking water as compared to those fed on oldman saltbush alone or supplemented with dry feedstuffs (i.e. concentrate feeds and straw). This association is not an option with saline lands since cactus cannot grow under saline conditions (water or soil). 7.3. Digestion of oldman saltbush diets The OM and CP digestibility of oldman saltbush alone ranges from 48 to 72% and from 49 to 83%, respectively (Table 6). These important variations could be due to the different ages, phenological stages of oldman saltbush at the time of harvest since the previous cutting (i.e. regrowth). The high solubility of oldman saltbush nitrogen could be the reason for the high CP digestibility reported in most studies. Weston et al. (1970) measured nutrient digestibilities, flow of digesta and their constituents through the rumen and abomasums and the concentrations of end-products of digestion by sheep fed oldman saltbush foliage. They noted that oldman saltbush CP was extensively degraded to ammonia in the rumen and accordingly the protein value of the diet was much lower than indicated by its digestible CP content. This study showed also that the ruminal absorption of volatile fatty acids was impaired and that 72% of the dietary nitrogen intake left the rumen as non ammonia nitrogen. The loss of dietary N during passage through the rumen was ascribed to microbial deamination of dietary nitrogenous substances. This was reflected in the presence of significant quantities of ammonia in the rumen. Ammonia levels in the rumen were in the order of 27 ± 3 mg N/100 mL. The overall digestibility of dietary N was in the order of 76%. The low energy value of oldman saltbush (6–8 MJ ME/kg DM) limit the transformation of the excessive concentration of ammonia N into microbial proteins. The disequilibrium between oldman saltbush energy and protein results in negative N balance in sheep and goats fed on this shrub species alone. However, when an energy source, e.g. barley, was associated to oldman saltbush, sheep and goats retained from 6 to 13 g N/day depending on the amount and the source

23

of energy added to the diet. Du Toit et al. (2006) supplemented oldman saltbush with increasing levels of barley or maize (0, 15, 30 and 45%). They noted that irrespective to the type of supplement, supplementation of oldman saltbush with energy tended to increase rumen fermentation. Rumen ammonia concentration decreased at the 30% level of supplementation probably as a result of an improvement of microbial protein synthesis. Total rumen VFA increased with increasing levels of both barley and maize supplementation. It is concluded from this study that supplementing sheep with barley and maize at 30% level increased fermentation in the rumen of sheep fed on oldman saltbush and enhanced utilisation of degradable protein available in the rumen. 7.4. Animal performance Productive and reproductive performances of ruminants depend mainly on nutrient supply and utilisation and the presence of secondary compounds. It is clear from the previous discussion that oldman saltbush is relatively low in energy and true protein but high in salt and oxalates. These characteristics could explain the loss of the body weight of sheep and goats when fed on oldman saltbush alone. 7.4.1. Growth and meat quality Table 6 shows that sheep fed oldman saltbush foliage alone decreased or, at best, maintained liveweight. However, the provision of barley would improve considerably the growth rate of sheep. Grazing herbaceous vegetation and receiving cactus cladodes, sheep on oldman saltbush grew at a rate of 100 g/day (Le Houérou, 1992). This feeding regimen is cost-effective and represents a promising alternative for livestock living in dry areas. Meat from sheep grazing saltbush rich in vitamin E oxidised at a slower rate than meat from sheep grazing adjacent crop stubble, thus increasing the retail shelf life of the saltbush meat (Pearce et al., 2005). Synthetic betaines are used as an ingredient in many feedlot rations and levels that are comparable to natural levels in oldman saltbush may lower subcutaneous fat deposits and improve meat quality. 7.4.2. Milk production The response of dairy ewes or goats to oldman saltbush feeding was seldom investigated. Abu-Zanat and Tabbaa (2006) studied the effect of feeding a diet containing airdried saltbush (mixture of Atriplex halimus and oldman saltbush) growing in Jordan on the milk yield of Awassi ewes and growth rate of their lambs. They compared three diets composed of concentrate and shredded barley straw, concentrate and 50% straw:50% saltbush, or concentrate and 100% saltbush. These diets were used because, under Jordanian conditions, substituting saltbush for barley straw in diets of sheep will reduce the cost of roughage component. The diets had no significant effect on milk production, birth weight, weaning weight or growth rates of lambs. These authors concluded that feeding Atriplex browse with concentrate did not cause any significant

24

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

problems on milk yield or growth rate of lambs. A similar conclusion was reached by Chadwick et al. (2009) who found that lamb birth weight and pre-weaning growth rates were not affected by feeding ewes a combination of saltbush, annual pasture, and barley and lupin grain. However, special attention should be taken when feeding saltbush to lactating Awassi ewes for long periods since selenium level in the blood serum of ewes fed saltbush might exceed normal levels (Aazzeh and Abu-Zanat, 2004). We are not aware of any literature data on the effect of oldman saltbush feeding on milk quality in ruminants, except for recent data (Chadwick et al., 2009) on the mineral composition of ewe milk. Ewes grazing saltbush had a higher total mineral content in their milk at 3 weeks into lactation than pasture-fed ewes, with higher concentrations of K, Mn, B, P and Zn (and lower Al and Fe concentrations). 7.4.3. Wool growth The opportunity to improve wool growth efficiency in sheep through increased dietary salt has received little attention despite studies indicating this may be a feasible strategy. Thomas et al. (2007b) found that sheep consuming diets high in sodium chloride grew more wool per unit of digestible organic matter intake. In addition to the effect of salt, high sulphur in oldman saltbush may improve wool growth (Franklin-McEvoy et al., 2007; Norman et al., 2009a). 8. Utilisation modes of oldman saltbush for sheep and goat feeding Different forms of feeding oldman saltbush are reported in the literature. These include free grazing, cut-and-carry technique and feeding as fresh, dried or ensiled material. 8.1. Free grazing vs. cut and carry Feeding a high-energy supplement such as barley can improve the feeding value of saltbush pastures by providing energy to ruminal microbes to produce microbial protein, stimulate carbohydrate digestion and detoxify secondary compounds (Hassan and Abdel-Aziz, 1979; Benjamin et al., 1992; Van der Baan et al., 2004; Norman et al., 2008). While several pen feeding trials demonstrated complementarity between saltbush and low energy and low salt feeds (Warren et al., 1990), animals offered straw while grazing oldman saltbush in the field have not demonstrated higher productivity than animals without supplements (Franklin-McEvoy et al., 2007; Norman et al., 2008). Recent work by Thomas et al. (2007a) examined the diet selection of penned sheep offered choices between high-salt and high-energy diets, and a range of low-salt diets of differing energy and protein levels. They concluded that supplements high in energy are more likely to be consumed by sheep grazing saltbush than roughage supplements. Additionally, they suggested that supplements of roughage should have DOMD values of between 0.52 and 0.60 for complementarity with the high salt diet, where sheep can choose their diet.

8.2. Oldman saltbush as alternative feed supplement Since oldman saltbush has a low ME value but is high in salt, sulphur and oxalates and induces mineral imbalances in animals, it should be considered as a supplement rather than a feed to be fed in a monoculture. The relative advantages of oldman saltbush as a supplement are that it produces biomass with high CP, vitamin E, and S during the summer/autumn period and this complements senesced pastures or poor quality crop stubbles. The key to utilisation is to achieve intake of oldman saltbush and the poor quality feed and as discussed previously this can be difficult to achieve (Franklin-McEvoy et al., 2007; Norman et al., 2008). Burritt and Provenza (2000) stated that “a varied diet should enhance animal’s ability to meet its nutritional needs when foraging on plants with secondary compounds as long as the toxins have different physiological effects, are detoxified by different metabolic pathways and do not interact to become more toxic.” There is an opportunity to improve the utilisation of oldman saltbush through a greater understanding of the secondary compounds present in the plant and through introduction of complementary shrubs or supplements. Wilson (1966) found that adding small amounts of oldman saltbush to a poor quality basal diet (DMD 53%) increased the digestibility of the diet and animals lost less weight than if they had the basal diet alone. Attempts have been made by several scientists to enhance the benefit from integrating oldman saltbush into livestock feeding. The relatively high CP content of oldman saltbush foliage encouraged the use of this shrub species as alternative N supplement for sheep, thus to reduce feeding cost. Nefzaoui et al. (2000) replaced soyabean meal (65 g) in equivalent CP by oldman saltbush (770 g) or Atriplex halimus (740 g) foliage given as supplements to Barbarine lambs fed on cactus-based diets. While lambs receiving soyabean meal grew at a rate of 70 g/day, a similar rate was attained with those supplemented with oldman saltbush or A. halimus (74 and 58 g/day, respectively). In another trial conducted in Tunisia, Ben Salem et al. (2004) showed that spineless cactus could replace the equivalent energy from a barley supplement while oldman saltbush could replace the equivalent CP from soyabean meal. The average daily gain of Barbarine lambs fed on straw-based diet and supplemented with barley and soyabean meal, barley and oldman saltbush, cactus and soybean meal, or cactus and oldman saltbush was 108, 59, 119 and 81 g/day, respectively. These two trials suggest that in presence of sufficient energy in the diet, oldman saltbush could replace soyabean meal. Cereal straws are produced in high quantities in many countries, particularly in the WANA region and southern Australia. Since the 1980s, landholders in the WANA region have treated fibrous crop residue with anhydrous ammonia or urea to improve the nutritive value. However, the adoption of this technique in the region is still limited. Ben Salem et al. (2002b) tested the hypothesis as to whether feeding oldman saltbush could replace urea treatment of straw. The amount of oldman saltbush foliage used contains the same amount of CP as that obtained by urea treatment of straw. Sheep receiving cactus ad libitum and supplemented

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

with either untreated barley straw (US), urea treated straw (UTS) or oldman saltbush and US grew at a rate of 8, 20 and 31 g/day. This study showed that N supplementation of cactus-based diets with UTS or oldman saltbush improved the feeding value of these diets and consequently sheep growth. A cactus-based diet, supplemented with oldman saltbush, promoted similar growth in sheep as the commonly used diet (US+ concentrate). 8.3. Feeding as fresh, dried or ensiled material Most in vivo studies on the evaluation of the nutritive value of oldman saltbush diets have been carried on penned sheep or goats. This is because the measurement of feed and water intakes and the determination of diet digestibility and N balance are easier in stall-fed than grazing animals. Generally, freshly cut or air-dried edible parts (leaves and twigs) of oldman saltbush were distributed to animals as the main diet or as supplement of low quality feed resources (e.g. cereal straws or stubbles and native pastures). According to Le Houérou (1992) air-drying would improve the palatability of oldman saltbush foliage, thus increases its intake by sheep. Ensiling shrub foliage is not a common technique among farmers from arid and semi-arid areas worldwide. This is a labour demanding and costly technique and is time consuming. In Egypt, Abou El Nasr et al. (1996) compared the nutritive value and sheep performances fed on oldman saltbush foliage distributed either as freshly cut, air-dried or ensiled material. While fresh foliage of oldman saltbush permitted to sheep to meet their maintenance requirements, sheep receiving air-dried oldman saltbush lost considerably body weight (−109 g/day). However, ensiled oldman saltbush exhibited the highest growth rate (91 g/day). This trend was supported by the good quality of the silage and the higher voluntary intake of DM, CP and NDF. It is unlikely that ensiling will be adopted in Australia due to high labour costs. 8.4. Shrub mixed diets The complementary role between shrubs could be a solution to make better use of oldman saltbush in livestock feeding. Shrubs mixed diets for ruminants have been used to overcome forage shortage during dry seasons (Le Houérou, 1992). Moreover, feeding animals with shrub mixed diets seems to be a recommended practice to dilute the negative effects of possible anti-nutritive factors (tannins, oxalates, etc.). Ben Salem et al. (2002c) supplemented a tanniniferous legume shrub (Acacia cyanophylla Lindl. syn. Acacia saligna) with barley (B) or spineless cactus cladodes (C, as energy sources) with (B+ oldman saltbush and C+ oldman saltbush) or without oldman saltbush (as N source). Supplementation of acacia with the mixture B+ oldman saltbush or C+ oldman saltbush increased microbial N synthesis in Barbarine lambs and growth rate (54 and 28 g/day, respectively) as compared to diets not supplemented with oldman saltbush (15 g/day and −54 g/day for lambs supplemented with only barley or cactus, respectively). Le Houérou (1991) evaluated a set of diets composed of one or more shrub species (Acacia

25

cyanophylla, Atriplex halimus, oldman saltbush, Artemisia herba alba, Atriplex canescens, Acacia ligulata and cactus cladodes) on stall-fed or free grazing sheep. The main merits of this experiment are its long duration (up to 238 days) and the large number of animals involved (460 ewes). This study showed that diets based on the foliage of only one shrub species without supplementation or complementary pasture are unable to meet nutrient requirements for grazing animals. Shrub curing increased substantially their intake. The increased intake could be explained: (i) in the case of Atriplex spp. like oldman saltbush by the reduction of the salt bearing glandular hair from the leaf surface during the curing and manipulation process, thus rendering the forage less saline, and more edible, (ii) the long duration of the experiment is an important factor since intake increased with time. Consumption after 3–5 months reached 1.5 to over 2.0 times the initial intake and much more in some species of Atriplex like oldman saltbush (4 times the initial intake) and (iii) the synergetic effect when two or three shrubs are mixed together in the ration. The combination of free grazing with pen supplementation of shrubs resulted in significant weight increase. According to Le Houérou (1991), the consumption of 2 kg DM of Atriplex corresponds with an ingestion of 500–600 g of ash and 120–140 g Na (300–350 g NaCl) per animal/day. It means that approximately 20 g of water are required for livestock to excrete 1 g of NaCl or 50 g for 1 g of N. This could become a limiting factor to the use of oldman saltbush in dry areas suffering from the permanent availability of water sources, or where the water available contains a high salt content itself. In this case, oldman saltbush plantation should be coupled with cactus plantations, or located within a radius of 2–3 km from permanent water. But in biosaline lands where only salt-tolerant species like oldman saltbush can grow, feeding mixed diets would involve supplementation or allowing animals into adjacent, non-saline, pastures. The incorporation of small amounts of tanniniferous foliage (e.g. Acacia cyanophylla foliage) in protein-rich diets increased lamb growth as a result of increased bypass proteins which is induced by tannins and protein interaction (Ben Salem et al., 2005b). This was not the case with oldman saltbush. Indeed, the association of incremental levels of air-dried Acacia cyanophylla foliage (0, 75, 150 and 225 g) with ad libitum oldman saltbush (freshly cut foliage) did not increase the average daily gains of Barbarine lambs. The high solubility of oldman saltbush nitrogen means that true protein is low in this shrub. It is well documented that tannins interact with proteins, thus protecting them against rumen degradation. 8.5. Alley-cropping with oldman saltbush Grazing of cereal stubbles in the summer period is a common practice in North Africa, southern Australia and southern Spain. During this period green forage is scarce. The alley-cropping which consists of cereal cropping between the rows (10–40 m) of fodder shrubs (e.g. oldman saltbush, Acacia cyanophylla and cactus) proved to be an efficient technique for improving livestock performances. This technique was initiated in Libya in early 1980s then applied in other countries mainly Morocco, Tunisia

26

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

and Spain. Experiments in Spain have shown that such a system may increase the stocking rate to 3.3 ewes/ha/yr with a net production of 50 kg live weight/ha/yr, which is 3 times higher than in the local traditional system of range-stubble-fallow and that lactating ewes maintain a high productivity without any external supplementation (Correal et al., 1990; Otal et al., 1992). Successful barleyoldman saltbush alley-cropping was reported in Morocco and its adoption and impact on farms’ conditions were assessed by Laamari et al. (2005). About third of farmers from the Irzain community in northeast Morocco adopted the technology on nearly a quarter of the land in this community. Barley grain and straw yields were 17% and 97% higher, respectively, in alley-cropping system than in the traditional barley-fallow system. Adopting oldman saltbush alley-cropping also meant that farmers had to buy less feed for their animals, reducing feed cost by 33% on the average. Using the SCUAF (Soil Changes under Agroforestry) model to assess the environmental impacts of alley-cropping systems over 15 yrs, the alley-cropping systems compared to farmers’ usual land-use practices, reduced loss and greatly improved soil organic carbon levels (CGIAR, 2006). Briefly, it is clear that oldman saltbush alley-cropping could greatly reduce soil erosion, restore soil organic matter, boost crop yields, and provide high returns on farmers’ investments. 9. Conclusions The potential of oldman saltbush has been recognised for many years across a variety of farming systems; however further planting can be expected given expanding salinity and aridity problems. One of the best attributes of oldman saltbush is its ability to grow and produce biomass in arid and saline environments. The C4 growth pattern of oldman saltbush complements annual pasture systems that have feed shortages during the hot months. Once established, the plants are hardy and may remain productive for a number of decades. High crude protein, vitamin E, and S complements senesced pastures or poor quality roughage. The major limitations of oldman saltbush are high salt (limiting VFI and reducing digestibility of the diet) and oxalates, moderate energy values, low levels of biomass production and the possibility of inducing mineral imbalances (such as Ca or Cu deficiency and S toxicity). Oldman saltbush is best considered as a supplement rather than forage to be fed as a sole diet. Ruminants grazing oldman saltbush require high-energy and low-salt feeds to complement the feeding value of oldman saltbush. As a supplement, saltbush has high value as a palatable source of minerals, antioxidants and CP. Mixing oldman saltbush with complementary shrubs like cactus cladodes is a feasible solution to enhance livestock performances. But, this supposes that associated shrubs (e.g. cactus, etc.) can grow on saline lands or established with oldman saltbush on non saline soils. The presence of vitamin E and betaine may also lead to improved meat quality. A better understanding of the variation in growth and feeding value of different oldman saltbush ecotypes may offer an opportunity to select improved lines of oldman saltbush for increasing productivity in a range of grazing systems. Alley-cropping with

oldman saltbush is a promising and simple technique that could be easily adopted by farmers. References Aazzeh, A.Y., Abu-Zanat, M.M., 2004. Impact of feeding saltbush (Atriplex sp.) on some mineral concentrations in the blood serum of lactating Awassi ewes. Small Rumin. Res. 54, 81–88. Abdul-Halim, R.K., Al-Badri, F.R., Yasin, S.H., Ali, A.T., 1990. Survival and productivity of chenopods in salt-affected lands of Iraq. Agric. Ecosyst. Environ. 31, 77–84. Abou El Nasr, H.M., Kandil, H.M., El Kerdawy, A., Dawlat, Khamis, H.S., El Shaer, H.M., 1996. Value of processed saltbush and acacia shrubs as sheep fodders under the arid conditions of Egypt. Small Rumin. Res. 24, 15–20. Abu-Zanat, M.W., Al-Hassanat, F.M., Alawi, M., Ruyle, G.B., 2003. Oxalate and tannins assessment in Atriplex halimus L. and Atriplex nummularia L. J. Range Manage. 56, 370–374. Abu-Zanat, M.W., Ruyleb, G.B., Abdel-Hamid, N.F., 2004. Increasing range production from fodder shrubs in low rainfall areas. J. Arid Environ. 59, 205–216. Abu-Zanat, M.M.W., Tabbaa, M.J., 2006. Effect of feeding Atriplex browse to lactating ewes on milk yield and growth rate of their lambs. Small Rumin. Res. 64, 152–161. Aguer, D., 1973. Compte rendu d’un essai de pâturage d’Atriplex par des béliers à Bou Rebia Août-Septembre 1972. Ministère de l’Agriculture/INRAT, Laboratoire de Zootechnie. 20 pp. Allison, M.J., Littledike, E.T., James, L.F., 1977. Changes in ruminal oxalate degradation rates associated with adaptation to oxalate ingestion. J. Anim. Sci. 45, 1173–1179. Arieli, A., Naim, E., Benjamin, R.W., Pasternak, D., 1989. The effect of feeding saltbush and sodium chloride on energy metabolism in sheep. Anim. Prod. 49, 451–457. Barrett-Lennard, E.G., 2003. The interaction between water logging and salinity in higher plants: causes, consequences and implications. Plant Soil 253, 35–54. Beadle, N.C.W., Whalley, R.D.B., Gibson, J.B., 1957. Studies in halophytes: 2. analytic data on the mineral constituents of three species of Atriplex and their accompanying soils in Australia. Ecology 38, 340–344. Ben Ameur, M., Blomeyer, A., 1974. Composition chimique et valeur alimentaire des fourrages grossiers. INRAT 1974. Ben Salem, H., 1998. Effet de l’Acacia cyanophylla Lindl. sur l’ingestion et la digestion des régimes destinés aux ovins. Rôle des tanins et perspectives d’amélioration de sa valeur alimentaire. Thèse Doctorat, Université de Dijon, France. 252 p. Ben Salem, H., Abdouli, H., Nefzaoui, A., El-Mastouri, A., Ben Salem, L., 2005a. Nutritive value, behaviour and growth of Barbarine lambs fed on oldan saltbush (Atriplex nummularia L.) and supplemented or not with barley grains or spineless cactus (Opuntia ficus indica f. inermis) pads. Small Rumin. Res. 59, 229–238. Ben Salem, H., Makkar, H.P.S., Nefzaoui, A., Hassayoun, L., Abidi, S., 2005b. Benefit from the association of small amounts of tannin-rich shrub foliage (Acacia cyanophylla Lindl.) with soya bean meal given as supplements to Barbarine sheep fed on oaten hay. Anim. Feed Sci. Technol. 122, 173–186. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2000. Supplementing range goats in central Tunisia with feed blocks or a mixture of Opuntia ficus indica f. inermis and Atriplex nummularia L. Effects on behavioural activities and growth. In: Proc. 7th International Conference on Goats, Tours, France, pp. 988–989. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2002a. Opuntia ficus indica f. inermis and Atriplex nummularia L. Two complementary fodder shrubs for sheep and goats. Acta Horticul. 581, 333–341. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2002b. Supplementing spineless cactus (Opuntia ficus indica f. inermis) based diets with ureatreated straw or oldman saltbush (Atriplex nummularia). Effects on intake, digestion and sheep growth. J. Agric. Sci. Cambr. 138, 85– 92. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2002c. Supplementation of Acacia cyanophylla Lindl. foliage-based diets with barley or shrubs from arid areas (Opuntia ficus indica f. inermis and Atriplex nummularia L.) on growth and digestibility in lambs. Anim. Feed Sci. Technol. 96, 15–30. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2004. Spineless cactus (Opuntia ficus indica f. inermis) and oldman saltbush (Atriplex nummularia L.) as alternative supplements for growing Barbarine lambs given strawbased diets. Small Rumin. Res. 51, 65–73. Benjamin, R.W., Orshan, G., G., Ronen, A., Lavie, Y., Barkai, D., Hefetz, Y., 1990. Effect of water availability (competition from annual vegeta-

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28 tion) and seasonal grazing on shrub regrowth. In: Benjamin, R.W., Seligman, N.G., Forti, M., Becker, K. (Eds.), Analysis of animal nutrition in shrub-grassland grazing systems with special reference to semi-arid Africa, semi-annual (August 1989-April 1990) Report, No BGUN-ARI-37–90, pp. 2–45. Beer Sheva: The Institutes for Applied Research, Ben Gurion University of the Negev. 77 pp. Benjamin, R.W., Lavie, Y., Forti, M., Barkai, D., Yonatan, R., Hefetz, Y., 1995. Annual regrowth and edible biomass of tow species of Atriplex and of Cassia sturtii after browsing. J. Arid Environ. 29, 63–84. Benjamin, R.W., Oren, 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. Bird, P.R., 1972. Sulphur metabolism and excretion studies in ruminants. 10. Sulphide toxicity in sheep. Aust. J. Biol. Sci. 25, 1087–1098. Burritt, E.A., Provenza, F.D., 2000. Role of toxins in intake of varied diets by sheep. J. Chem. Ecol. 26, 1991–2005. Chadwick, M.A., Williams, I.H., Vercoe, P.E., Revell, D.K., 2009. Feeding pregnant ewes a high-salt diet or saltbush suppresses their offspring’s postnatal renin activity. Animal 3, 972–979. Chriyaa, A., Boulanouar, B., 2000. Browse foliage as a supplement to wheat straw for sheep. In: Gintzburger G., Bounejmate, M., Nefzaoui, A. (Eds.). 2000. Fodder shrub development in arid and semi arid zones. Proc. workshop on native and exotic fodder shrubs in arid and semi-arid zones, 27 October–2 Nov 1996, Hammamet, Tunisia. ICARDA, Aleppo, Syria. Vol II: viii+pp 293–679. pp. 476–484. CGIAR, 2006. Science Council Brief, Standing Panel on Impact Assessment, number 12, issue October 2006. Correal, E., Robledo, A., Ripos, S., 1992. Grazing use of shrub plantations. 43rd Annual Meeting of the EAAP, Madrid 14–17 September 1992. pp 98–118. Correal, E., Otal, J., Sotomayor, J.A., 1990. Effects of grazing frequency and cutting height on the production of browsing biomass of oldman saltbush (Atriplex nummularia L.) in southeast Spain. In: Development and preservation of low input Mediterranean pastures and fodder systems. Proc. 6th Meeting of the FAO European Sub-Network on Mediterranean Pastures and fodder crops, 17–19 October, Bari, Italy, pp. 153–156. Correal, E., Stomayor, J.A., 2000. Effect of straw supplementation on intake and browsing of Atriplex nummularia (Oldman saltsbush) by Segurena ewes, Ander pen-feeding and free-grazing conditions. In Gintzburger G., M. Bounejmate, A. Nefzaoui (Eds.) 2000. Fodder shrub development in arid and semi-arid zones. Proc. Workshop on native and exotic fodder shrubs in arid and semi-arid zones, 27 Oct-2 Nov 1996, Hammamet, Tunisia. ICARDA, Aleppo, Syria. Vol II: viii + pp 293–679. 551–557. Cymbaluk, N.F., Miller, J.D., Christensen, D.A., 1986. Oxalate concentration in feeds and its metabolism by ponies. Can. J. Anim. Sci. 66, 1107–1116. Dalley, D.E., Isherwood, P., Skyes, A.R., Robson, A.B., 1997. Effect of intraruminal infusion of potassium on the site of magnesium absorption within the digestive tract in sheep. J. Agric. Sci., Cambr. 129, 99–105. David, A.M., 1981. The oxalate, tannin, crude fibre, and crude protein composition of young plants of some Atriplex species. J. Range Manage. 34, 329–331. De Kock, G.C., 1980. Drought resistant fodder crops. In: H.N. Le Houérou (Ed.), Browse in Africa. The current state of knowledge. Proc. Int. Symp. Browse in Africa, Addis Ababa, April 8–12, 1980. pp. 1–30. Dumancic, D., Eskileh, M., Le Houérou, H.N., 1982. Study on fodder shrubs consumption by sheep in Wishtata Range Development Project. Report No LIB 18, FAO, Tripoli, Libya. 11 p. Du Toit, C.J.L., van Niekerk, W.A., Hassan, A., Rethman, N.F.G., Coertze, R.J., 2006. Fermentation in the rumen of sheep fed Atriplex nummularia cv. De Kock supplemented with incremental levels of barley and maize. South Afr. J. Anim. Sci. 36, 74–77. FAO/WHO, 1973. Energy and protein requirements. FAO Nutritional Meeting Rep. Ser. No 52, WHO Tech. Rep. Ser. No 522 FAO, Rome, Italy. 127 p. Franklin-McEvoy, J., Bellotti, W.D., Revell, D.K., 2007. Supplementary feeding with grain improves the performance of sheep grazing saltbush (Atriplex nummularia) in autumn. Aust. J. Exp. Agric. 47, 912– 917. Franklin-McEvoy, J., Jolly, S., 2006. Towards a better understanding of animal nutrition in pastoral South Australia. Proc. Australian Rangelands Society Conference, Renmark, Australia, pp 155–158. Freer, M., Moore, A.D., Donnelly, J.R., 1997. GRAZPLAN: decision support systems for Australian enterprises-II. The Animal biology model for feed intake, production and reproduction and the GrazFeed DSS. Agric. Syst. 54, 77–126. Ghassemi, F., Jakeman, A.J., Nix, H.A., 1995. Salinisation of Land and Water resources. CAB International, Wallingford.

27

Guevara, J.C., Allegretti, L.I., Paez, J.A., Estevez, J.A., Le Houérou, H.N., Silver Colomer, J.H., 2008. Arid Land Res. Manage 19, 327–340. Hassan, N.I., Abdel-Aziz, H.M., 1979. Effect of barley supplementation on the nutritive value of saltbush (Atriplex nummularia). World Rev. Anim. Prod. XV, 47–55. Hassan, N.I., Abdel-Aziz, H.M., El Tabbakh, A.E., 1979. Evaluation of some forages introduced to newly reclaimed areas in Egypt. World Rev. Anim. Prod. 15, 31–35. ˜ ˜ Hirsch-Reinshagen, P., Canas, R., Bascunan, J., Lacher, E., 1986. Alimentos chilenos de uso pecuario contenido en nutrients brutos, digestibles y metabolizables para distintas especies. Ciencia de Investigación Agraria 3, 1–50. INRA, 1978. Alimentation des Ruminants. Ed. INRA Publications (Route de Saint-Cyr), 78000 Versailles. 621 p. James, L.F., Butcher, J.E., 1972. Halogeton poisoning of sheep: effect of high level oxalate intake. J. Anim. Sci. 35, 1233–1238. James, L.F., 1977. Oxalate poisoning in livestock. In: Keeler, R.F., Van Kampen, K.R., James, L.F. (Eds.), Effects of Poisonous Plants on Livestock. Academic Press, New York, N.Y. USA, pp. 135–145. Kaitho, R.J., Nsahlai, I.V., Williams, B.A., Umunna, N.N., Tamminga, S., Van Bruchem, J., 1998. Relationship between preference, rumen degradability, gas production and chemical composition of browses. Agrofor. Syst. 39, 129–144. Kandil, H.M., El Shaer, M.H., 1989. The utilization of Atriplex nummularia by goats and sheep in Sinai. In: E.S.E. Galal, M.B. Aboul-Ela, M.M. Shafie (Eds.), Ruminant production in the dry subtropics: Constraints and potential. Proc. Int. Symp., Cairo, November 1988, EAAP Publications, No 38, Wageningen, Netherlands. pp. 71–73. Khalil, J.K., Sawaya, W.N., Hyder, S.Z., 1986. Nutrient composition of Atriplex leaves grown in Saudi Arabia. J. Range Manage. 39, 104–107. Kumara Mahipala, M.B.P., Krebs, G.L., McCafferty, P., Gunaratne, L.H.P., 2009. Chemical composition, biological effects of tannin and in vitro nutritive value of selected browse species grown in the West Australian Mediterranean environment. Anim. Feed Sci. Technol., doi:10.1016/j.anifeedsci.2009.06.014. Laamari A., Boughlala M., Chriyaa A., 2005. Adoption and impact studies in Morocco. In: Shideed Kamil H. and Mohamed El Mourid (eds.). Adoption and impact assessment of improved technologies in crop and livestock production systems in the WANA region. The development of integrated Crop/Livestock Production in Low Rainfall Areas of Mashreq and Maghreb Regions (Mashreq/Maghreb Project). ICARDA, Aleppo, Syria, viii+160 pp. En. pp. 107–118. Le Houérou, H.N., 1965. Les cultures fourragères en Tunisie. Document Technique No 13, INRA, Tunis, Tunisia. 81 p. Le Houérou, H.N., 1986. Salt tolerant plants of economic value in the Mediterranean basin. Reclam. Reveg. Res. 5, 319–341. Le Houérou, H.N., 1991. Feeding shrubs to sheep in the Mediterranean arid zone: intake, performance and feed value. IV Congrès International des Terres de Parcours, Montpellier, France 1991. 623–628. Le Houérou, H.N., 1992. The role of saltbushes (Atriplex spp.) in arid land rehabilitation in the Mediterranean basin: a review. Agrofor. Syst. 18, 107–148. Le Houérou, H.N., Gintzburger, G., El Khoja, N., 1982. Chemical composition and nutritive value of some range plants and fodder shrubs of Libya. FAO/UTFN/Project LIB/018. Technical Paper N◦ 44, November 1982. Le Houérou, H.N., Pontanier, R., 1987. Les plantations sylvo-pastorales dans la zone aride de la Tunisie. Notes Techniques du MAB 18, 11– 81. Makkar, H.P.S., francis, G., Becker, K., 2007. Bioactivity of phytochemicals in some lesser-known plants and their effects and potential applications in livestock and aquaculture production systems. Animal 1, 1371–1391. Masters, D., Tiong, M., Norman, H., Vercoe, P., 2009. The mineral content of river saltbush (Atriplex amnicola) changes when sodium chloride in the irrigation solution is increased. In: T.G. Papachristou, Z.M. Parissi, H. Ben Salem, P. Morand-Fehr (Eds.), Nutritional and foraging ecology of sheep and goats. Zaragoza: CIHEAM, FAO, NAGREF. 2009, 491 p. Options Méditerranéennes, Série A: Mediterranean Seminars, No. 85. pp. 153–164. Masters, D.G., Benes, S.E., Norman, H.C., 2007. Biosaline agriculture for forage and livestock production. Agric., Ecosyst. Environ. 119, 234–248. Masters, D.G., Norman, H.C., Barrett-Lennard, E.G., 2005a. Agricultural systems for saline soil: the potential role of livestock. Asian Aust. J. Anim. Sci. 18, 296–300. Masters, D.G., Rintoul, A.J., Dynes, R.A., Pearce, K.L., Norman, H.C., 2005b. Feed intake and production in sheep fed diets high in sodium and potassium. Aust. J. Agric. Res. 56, 427–434. Mayberry, D.E., Masters, D.G., Vercoe, P.E., 2009. Saltbush (Atriplex nummularia L.) reduces efficiency of rumen fermentation in sheep. In: T.G.

28

H. Ben Salem et al. / Small Ruminant Research 91 (2010) 13–28

Papachristou, Z.M. Parissi, H. Ben Salem, P. Morand-Fehr (Eds.), Nutritional and foraging ecology of sheep and goats. Zaragoza: CIHEAM, FAO, NAGREF. 2009, 491 p. Options Méditerranéennes, Série A: Mediterranean Seminars, No. 85. pp. 245–249. McDowell, L.R., 1992. Minerals in Animal and Human Nutrition. Academic Press Inc, San Diego. McDowell, L.R., 2003. Minerals in Animal and Human Nutrition, second edition. Elsevier, 644 p. Morcombe, P.W., Young, G.E., Boase, K.A., 1996. Grazing a saltbush (Atriplex-Maireana) stand by Merino wethers to fill the ‘autumn feedgap’ experienced in the Western Australian wheat belt. Aust. J. Exp. Agric. 36, 641–647. National Land & Water Resources Audit 2001. Australian Dryland Salinity Assessment 2000. National Land & Water Resources Audit: Canberra, Australia. Nefzaoui, A., 2002. Rangeland management options and individual and community strategies of agropastoralists in central and Southern Tunisia. In: Ngaido, T., McCarthy, N., Di Gregorio, M. (Eds.), International Conference on Policy and Institutional Options for the Management of Rangelands in Dry Areas. Workshop summary paper. CAPRi Working Paper No. 23, Tunisia. Nefzaoui, A., Ben Salem, H., Ben Salem, L., 2000. Nitrogen supplementation of cactus-based diets fed to Barbarine yearlings. In: Gintzburger G., M. Bounejmate, M., A. Nefzaoui (Eds.). 2000. Fodder shrub development in arid and semi arid zones. Proc. workshop on native and exotic fodder shrubs in arid and semi-arid zones, 27 October–2 November 1996, Hammamet, Tunisia. ICARDA, Aleppo, Syria. Vol II: viii+pp 293–679. 512–517. Newton, G.L., Fontenot, J.P., Tucker, R.E., Polan, C.E., 1972. Effects of high dietary potassium intake on the metabolism of magnesium by sheep. J. Anim. Sci. 35, 440–445. Norman, H.C., Friend, C., Masters, D.G., Rintoul, A.J., Dynes, R.A., Williams, I.H., 2004. Variation within and between two saltbush species in plant composition and subsequent selection by sheep. Aust. J. Agric. Res. 55, 999–1007. Norman, H.C., Masters, D.G., Wilmot, M.G., Rintoul, A.J., 2008. Effect of supplementation with grain, hay or straw on the performance of weaner Merino sheep grazing old man (Atriplex nummularia) or river (Atriplex amnicola) saltbush. Grass and Forage Science 63, 179–192. Norman, H.C, Wilmot, M.G., Thomas, D.T, Barrett-Lennard, E.G., Masters, D.G., 2009a. Sheep production, plant growth and nutritive value of a saltbush-based pasture system subject to rotational grazing or setstocking. Small Rumin. Res. (This special issue). Norman, H.C., Revell, D.K., Mayberry, D.E., Rintoul, A.J., Wilmot, M.G., Masters, D.G., 2009b. Comparison of in vivo organic matter digestibility of native Australian shrubs to in vitro and in sacco predictions. Small Rumin. Res. (This special issue). Norman, H.C., Wilmot, M.G., Thomas, D.T., Masters, D.G., Revell, D.K., 2009c. Stable carbon isotopes accurately predict diet selection by sheep fed mixtures of C3 annual pastures and saltbush or C4 perennial grasses. Livest. Sci. 121, 162–172. Osman, A.E., bahhady, F., Hassan, N., Ghassali, F., Al Ibrahim, T., 2006. Livestock production and economic implications from augmenting degraded rangeland with Atriplex halimus and Salsola vermiculata in Northern Syria. J. Arid Environ. 65, 474–490. Otal, J., Belmonte, C., Correal, E., Sotomayor, J.A., 1992. Evaluation of sheep production under continuous rotational grazing of a saltbush plantation (Atriplex spp.) in southeast Spain. Proc. IV Int. Rangeland Congr., Montpellier. Papanastasis, V.P., Tiakoulaki, M.D., Decandia, M., Dini-Papanastasi, O., 2008. Integrating woody species into livestock feeding in the Mediterranean areas of Europe. Anim. Feed Sci. Technol. 140, 1–17. Pearce, K.L., Masters, D.G., Smith, G.M., Jacob, R.H., Pethick, D.W., 2005. Plasma and tissue ␣-tocopherol concentrations and meat colour stability in sheep grazing saltbush (Atriplex spp.). Aust J. Agric. Res. 56, 663–672. Playne, M.J., Echevarria, M.G., Megarrity, R.G., 1978. Release of nitrogen, sulphur, phosphorus, calcium, magnesium, potassium and sodium from four tropical hays during their digestion in nylon bags in the rumen. J. Sci. Food Agric. 29, 520–526. Plenchette, C., Duponnosis, R., 2005. Growth response of the saltbush Atriplex nummularia L. to inoculation with the arbuscular mycorrhizal fungus Glomus intraradices. J. Arid Environ. 61, 535–540. Provenza, F.D., 1995. Post ingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48, 2–17. Provenza, F.D., 1996. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J Anim. Sci. 74, 2010–2020.

Qureshi, R.H., Barrett-Lennard, E.G., 1998. Saline Agriculture for Irrigated Land in Pakistan: A Handbook. Australian Centre for International Agricultural Research, Canberra. Saadani, Y., Kayouli, C., Narjisse, H., 1989. Valeur nutritive d’un parcours mixte à Acacia cyanophylla, Atriplex nummularia et Medicago arborea. XVI Congrès International des Herbages, Nice, France, 1989. pp 943–944. Silva, E.S., Pereira, C.C., 1976. Aislacion y composicion de las proteinas de hojas de Atriplex nummularia y Atriplex repanda. Ciencia de Investigación Agraria 3 (4), 169–174. Silva-Colomer, J., Fonolla, J., Raggi, L.A., Boza, J., 1986. Valoracion nutritiva de Atriplex nummularia en ganado caprina. Rev. Argentina Prod. Anim. 6, 661–665. Standing Committee on Agriculture, 1990. Feeding Standards for Australian Livestock. CSIRO Publications, Melbourne. Tazi, M., Birouk, A., Hafidi, B., Aghlabi, M., 2000. Pâturage d’Atriplex nummularia dans la zone aride du sud du Maroc. In: Gintzburger G., M. Bounejmate, M. and A. Nefzaoui (Eds.). 2000. Fodder shrub development in arid and semi arid zones. Proc. workshop on native and exotic fodder shrubs in arid and semi-arid zones, 27 October–2 November 1996, Hammamet, Tunisia. ICARDA, Aleppo, Syria. Vol II: viii+pp 293–679. 570–579. Thomas, D.T., Rintoul, A.J., Masters, D.G., 2007a. Sheep select combinations of high and low sodium chloride, energy and crude protein feed that improve their diet. Appl. Anim. Behav. Sci. 105, 140–153. Thomas, D.T., Rintoul, A.J., Masters, D.G., 2007b. Increasing dietary sodium chloride increases wool growth but decreases in vivo organic matter digestibility in sheep across a range of diets. Aust. J. Agric. Res. 58, 1023–1030. Ulyatt, M.J., 1973. Chemistry and Biochemistry of Herbage. Academic Press, London, pp. 131–178. Underwood, E.J., Suttle, N.F., 1999. The Mineral Nutrition of Livestock, 3rd edition. CAB International, New York. Van der Baan, A., van Niekerk, W.A., Rethman, N.F.G., Coertze, R.J., 2004. The determination of digestibility of Atriplex nummularia cv. De Kock (Oldman’s saltbush) using different in vitro techniques. South Afr. J. Anim. Sci. 34, 95–97. Van Niekerk, W.A., Sparks, C.F., Rethman, N.F.G., Coertze, R.J., 2004a. Qualitative characteristics of some Atriplex species and Cassia sturtii at two sites in South Africa. South Afr. J. Anim. Sci. 34, 108–110. Van Niekerk, W.A., Sparks, C.F., Rethman, N.F.G., Coertze, R.J., 2004b. Mineral composition of certain Atriplex species and Cassia sturtii. South Afr. J. Anim. Sci. 34, 105–107. Warren, B.E., Bunny, C.L., Bryant, E.R., 1990. A preliminary examination of the nutritive value of four saltbush (Atriplex) species. Proc. Aust. Soc. Anim. Prod. 18, 424–427. Warren, B.E., Casson, T., 1992. Perfromance of sheep grazing salt tolerant forages on revegetated saltland. Proc. Aust. Soc. Anim. Prod. 19, 237. Watson, M.C., Banuelos, G.S., O’Leary, J.W., Riley, J.J., 1994. Trace element composition of Atriplex grown with saline drainage water. Agric. Ecosyst. Env. 48, 157–162. Watson, M.C., O’Leary, J.W., Glenn, E.P., 1987. Evaluation of Atriplex lentiformis (Torr.) S. Wats. and Atriplex nummularia Lindl. as irrigated forage crops. J Arid Environ. 13, 293–303. Watson, M.C., O’Leary, W.O., 1993. Performance of Atriplex species in the San Joaquin valley, California, under irrigation and with mechanical harvests. Agric. Ecosyst. Environ. 43, 255–266. Wehren, W., 1976. Eignung und futterwert, besonders aminosäurenzusammensetzung von unkonventionellen proteinquellen in semiariden gebieten Tunesiens. PhD. Thesis, University of Bohn, Bonn, Germany. Weston, R.H., Hogan, J.P., Hemsley, J.A., 1970. Some aspects of the digestibility of Atriplex nummularia (saltbush) by sheep. Proc. Aust. Soc. Anim. Prod. Vol. II, 517–521. White, C.L., Rewell, L., 2007. Vitamin E and selenium status of sheep during autumn in Western Australia and its relationship to the incidence of apparent white muscle disease. Aust. J. Exp. Agric. 47, 535–543. Wilmot, M., Norman, H., 2006. Saltbush biomass in a saline grazing system––use it or lose it. In: Adams, N. (Ed.), Animal Production in Australia. Proc. Aust. Soc. Anim. Prod. Biannual Conf., Perth Australia. Wilson, A.D., 1966. The value of Ariplex (Saltbush) and Kochia (Bluebush) species as food for sheep. Aust. J. Agric. Res. 17, 147–153. Wilson, A.D., 1974. Water consumption and water turnover of sheep grazing semi arid pasture communities in New South Wales. Aust. J. Agric. Res. 25, 339–347. Wilson, A.D., 1977. The digestibility and voluntary intake of the leaves of trees and shrubs by sheep and goats. Aust. J. Agric. Res. 28, 501–508.