Review article
A review of the potential of
Lathyrus sativus
L. and
L. cicera
L. grain for use as animal feed
C.D. Hanbury
a,*, C.L. White
b, B.P. Mullan
c, K.H.M. Siddique
a,caCentre for Legumes in Mediterranean Agriculture (CLIMA), University of Western Australia,
Nedlands 6907, Australia
bCSIRO, Division of Animal Production, Private Bag, PO Wembley 6014, Australia cAgriculture Western Australia, Locked Bag No. 4, Bentley Delivery Centre, Bentley 6983, Australia
Received 28 December 1999; received in revised form 3 July 2000; accepted 19 July 2000
Abstract
The use of two closely related species, Lathyrus ciceraand L. sativus, as grain legumes for human and animal consumption, dates to the Neolithic period. Due to its tolerance to harsh environmental conditionsL. sativusis still used widely for human food in Ethiopia and the Indian sub-continent, although cultivation has diminished in many other regions.
The grain of bothL. ciceraand L. sativus contains a neurotoxin, 3-(-N-oxalyl)-L-2,3-diamino
propionic acid (ODAP), which can cause a paralysis of the lower limbs (lathyrism). Due to the occurrence of lathyrism in humans recent plant breeding has produced cultivars with low ODAP concentrations. The susceptibility of animal species to lathyrism is poorly understood, although horses and young animals are more susceptible. Older published animal feeding studies are of limited use, since the presence and role of ODAP was unknown until the 1960s. More recent feeding studies indicate that low ODAP lines ofL. ciceraorL. sativuscan be safely incorporated at inclusion rates up to 40, 30 and 70% of the diet of poultry, pigs and sheep, respectively, without growth reductions.
The compositions of bothL. ciceraandL. sativusare similar to other commonly used feed grain legumes, respective protein contents are 25 and 27%. Antinutritional factors (ANFs), other than ODAP, are present in bothL. ciceraandL. sativusat concentrations similar to those found in other grain legumes; including trypsin inhibitors, chymotrypsin inhibitors, amylase inhibitors, lectins, tannins, phytate and oligosaccharides. The effect of ANFs inL. ciceraandL. sativuson animal performance is not well understood and sometimes confounded with ODAP effects. Heating of grain will reduce levels of the proteinaceous ANFs and in some cases ODAP as well.
Variation recorded in the germplasm ofL. ciceraandL. sativushas not been greatly utilised in plant breeding to lower levels of ANFs, with the exception of ODAP, leaving considerable potential for rapid improvement of cultivars. L. cicera and L. sativus are low production cost legumes
*Corresponding author. Tel.:61-8-9368-3744; fax:61-8-9368-2165
E-mail address: [email protected] (C.D. Hanbury).
0377-8401/00/$ ± see front matter#2000 Elsevier Science B.V. All rights reserved.
adapted to low rainfall environments and have considerable potential as good quality, cheap protein sources. As world demand for legume feed protein is likely to increase, due to increasing demand for animal food products, bothL. cicera and L. sativus are crops that should be considered in regions with suitable environments.#2000 Elsevier Science B.V. All rights reserved.
Keywords: Lathyrus; Protein; ODAP; Antinutritional factors; Lathyrism
1. Introduction
The use of legumes as sources of protein for the animal feed industry is expected to increase further in the near future. Rising incomes in the Asian region are increasing the demand for meat products, and hence the requirement for animal feeds. There have been changes in public perception and some unfortunate developments, such as the consequences of `mad cow' disease (i.e. bovine spongiform encephalopathy or BSE) in UK. This has resulted in many feed compounders either choosing to, or being banned from, using animal by-products as a source of protein (Farrell, 1997). The amino acid requirement of animals often differ with species and bodyweight, hence no single source of plant protein will provide the exact amino acids required for all animals. It is, therefore, preferable to include a range of protein sources in diet formulations, each complementing the other. For these reasons, the demand for grain legumes, such as
Lathyrusspp., by the feed industry is expected to increase. Any feedstuff is likely to be used in diets for animals if it supplies the required nutrients, if it is cost competitive with other available ingredients, and if the user is con®dent it will produce the desired result. Soybean (Glycine max) meal is used widely as a source of protein for animal feeds, and the price of most other protein meals and grain legumes are set relative to this commodity. In Europe there has been increasing emphasis on local production of legumes for animal feed in order to supply some of this protein demand (Gatel, 1994), rather than relying on imported soybean meal. Subsidies have resulted in increasing production of, particularly, ®eld peas (Pisum sativum) and faba beans (Vicia faba). This expansion has been partly at the expense of previously grown legume crops, such as Lathyrus spp., which do not have subsidies (Franco Jubete, 1991).
The genusLathyrusis a large one, comprising 189 species and sub-species according to Allkin et al. (1985), and approximately 150 species according to Kupicha (1983). Of these only a small number are cultivated. The closely relatedL. sativus(grass pea) andL. cicera(dwarf chickling) both belong to the same section: Lathyrus. Jackson and Yunus (1984) suggest that the similarities between semi-domesticated L. cicera and domesticated L. sativus may be a result of hybridisation or common ancestry. Some interspeci®c crosses between the two have been successful (Yunus and Jackson, 1991). Archaeobotanical evidence shows that bothL. sativusandL. cicerawere cultivated on the Iberian peninsula in the Neolithic period (PenÄa-Chocarro and Zapata PenÄa, 1999). Evidence also suggests thatL. sativus is possibly the most ancient domesticated crop in Europe, the Neolithic expansion of its cultivation into what is now Spain led to the cultivation of a local native species,L. cicera(Kislev, 1989). Erskine et al. (1994) suggest thatL. sativuswas originally domesticated as a secondary crop as a result of being a weed of lentil (Lens culinaris) crops.
2. Lathyrism
Lathyrusspecies, particularlyL. sativus, have been known since classical times to be implicated in a paralysis of humans and animals (Hugon et al., 2000) known as ``lathyrism'' or more speci®cally ``neurolathyrism''. Both ruminants and monogastric species can be affected, some literature indicates that monogastrics can be more affected. It was only in the later half of the 20th century that the compound responsible was identi®ed (Murti et al., 1964; Rao et al., 1964).
There are two forms of lathyrism, neurolathyrism and osteolathyrism. Osteolathyrism is characterised by skeletal deformities and can be caused by consumption of the species
L. odoratus(sweet pea),L. hirsutus,L. pusillusandL. roseus(Roy, 1981). Osteolathyrism has been recorded experimentally in a wide range of animals (Barrow et al., 1974). The principal compound responsible was found to beb-aminopropionitrile (BAPN; Fig. 1), although the related nitriles aminoacetonitrile (AAN) and methylene aminoacetonitrile (MAAN) also have some osteolathyritic activity (Barrow et al., 1974). Although BAPN is not found in eitherL. sativus or L. cicera (Bell, 1962, 1964), there is evidence that a BAPN precursor (2-cyanoethyl-isoxazolin-5-one) is present inL. sativusseedlings but not in seed (Lambein et al., 1993). Consumption of L. sativus seedlings and shoots as vegetables has been blamed as the cause of osteolathyritic symptoms found in a small proportion of people with chronic neurolathyrism (Haque et al., 1997). Incidents of osteolathyrism from feeding ofL. sativusorL. cicera have not been reported in animal studies, either under natural grazing or experimental conditions, and consequently the following discussion will focus on neurolathyrism.
Neurolathyrism is the term used to describe the symptoms shown after heavy consumption of several differentLathyrusspecies and someViciaspecies. The symptoms are weakness of the hind limbs and paralysis or rigidity of the muscles. Within the
Lathyrusgenus, the category of neurolathyrism has been further divided into two sub-categories. One is caused by the compoundL-2,4-diaminobutyric acid (DABA; Fig. 1),
et al., 1974). However, DABA is not found inL. ciceraor L. sativus(Bell, 1962, 1964; Padmanaban, 1980). The form of neurolathyrism most pertinent to this discussion is that caused by the non-protein amino acid 3-(-N-oxalyl)-L-2,3-diamino propionic acid (ODAP,
also referred to asb-N-oxalylamino-L-alanine or BOAA; Fig. 1): which has been recorded
in humans and animals following consumption ofL. sativus,L. cicera,L. ochrusandL. clymenum(Barrow et al., 1974; Padmanaban, 1980; Franco Jubete, 1991). The seed of a number of other uncultivatedLathyrusspecies have been found to contain ODAP (Bell, 1962, 1964). Historically the consumption ofL. sativushas been most often linked with lathyrism in humans and animals, primarily because of allLathyrusspecies it is the most widely utilised as grain and fodder. Lathyrism is the term mostly used to refer to neurolathyrism caused by ODAP, therefore this term will be used in this review from this point onward.
Lathyrism in humans has received more attention than that in animals, due to the social cost. Symptoms in humans are most often initial painful spasms in the muscles of the lower limbs with accompanying weakness, followed by chronic spastic paraplegia of various degrees (Spencer et al., 1986), and can lead to total loss of use of the legs (Attal et al., 1978). The paralysis is rarely reversible (and then only in early stages of the symptoms; Hugon et al., 2000) and the consequences for poor communities who depend uponL. sativus as a primary food source at times of food scarcity can be devastating. Lathyrism still occurs, with a 1997 outbreak during food shortages in Ethiopia crippling 2000 people (Getahun et al., 1999). Lathyrism is endemic to the areas of the world which have signi®cant areas ofL. sativus cultivation; India, Bangladesh, Ethiopia and Nepal. However, in the 20th century outbreaks were also reported in Afghanistan, Algeria, China, France, Germany, Italy, Pakistan, Romania, Russia, Spain and Syria (Trabaud and MouhaÈrram, 1932; Barrow et al., 1974; Roy and Spencer, 1989; Hugon et al., 2000).
Fig. 1. Chemical diagrams ofb-aminopropionitrile (BAPN),L-2,4-diaminobutyric acid (DABA), 3-(-N
Boiling has been found to reduce ODAP levels in several cases, however, there are mixed reports on other forms of cooking (Tekle Haimanot et al., 1993; Akalu et al., 1998). Padmajaprasad et al. (1997) reported that boiling grain and discarding the water reduced ODAP levels by up to 90%.
3. ODAP toxicity
Following its isolation and identi®cation (Murti et al., 1964; Rao et al., 1964) the neurolathyritic action of ODAP was soon demonstrated in adult monkeys (Macaca radiata; Rao et al., 1967). Cheema et al. (1969) administered ODAP intraperitoneally to rats. Young rats showed lathyrism symptoms and had 0.11mmol gÿ1ODAP in the brain, adult rats showing trace or nil ODAP and no symptoms. Olney et al. (1976) found some indication of exclusion of ODAP by the blood-brain barrier in mice. Padmanaban (1980) suggested that the hypothesis of less ODAP exclusion by the blood-brain barrier in young animals should be re-examined, as greater excretion of ODAP by older animals may be an important factor. Spencer et al. (1986) showed unequivocally that ODAP, either naturally present in L. sativus or when added to other food sources, was the cause of corticospinal dysfunction in monkeys (Macaca fascicularis), with symptoms of hind limb motor dif®culties.
ODAP acts as a glutamate (Fig. 1) analogue in the nervous system and probably acts by binding strongly to a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-type glutamate receptors. Permanent damage probably occurs with excitotoxic degeneration of neurons, although there are other possible neurotoxic effects. The ultimate fate of ODAP and the distribution in the brain and spinal cord is not known (Hugon et al., 2000). ODAP was not detected in pig loin tissue following feeding for an extended period (Castell et al., 1994; see Section 4.3).
In human populations young men are widely reported as the most susceptible to lathyrism (McCarrison, 1926; Shourie, 1945; Attal et al., 1978; Hamid et al., 1986; Getahun and Tekle Haimanot, 1997), although the reasons for this are not understood (Hugon et al., 2000). The production and susceptibility to ODAP may be linked to Zn de®ciency in plants and humans, respectively (Lambein et al., 1994; Lambein and Kuo, 1997). ODAP has also been found to inhibit growth of some insects and yeasts (Rao et al., 1964; Mehta et al., 1972), and so may have a plant protective role.
4. The nutritive value ofLathyrusfor animals
4.1. Chemical composition of the seed
Note: All concentrations in grain are expressed as received unless speci®ed otherwise.
4.1.1. Proximate composition
Table 1
Composition ofL. ciceraandL. sativusin comparison to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius)a
L. cicera L. sativus Field pea Faba bean Lupin
i ii iii iv Mean iii iv v vi vii viii ix x xi xii Mean i xiii i xiii i xiii
No. lines 1 1 4 1 ± 8 1 3 1 3 1 1 25 1 1 ± 1 24±3788 1 5±355 1 111±3782
Component(%DM)
Protein 21.7 27.2 33.0 26.4 29.6 34.3 30.1 30.9 26.4 32.6 26.3 31.3 27.3 35.9 26.9 29.4 21.0 25.7 23.7 26.9 29.1 35.1 Ash 2.9 3.1 3.8 3.1 3.5 3.9 3.1 3.3 2.8 2.6 3.2 3.1 2.0 2.7 2.9 2.6 3.3 2.8 3.8 3.0 2.6 3.0 Fat 1.4 0.7 ± ± 1.1 ± ± 0.9 1.7 5.3 0.7 1.0 1.4 1.2 0.8 1.6 1.7 1.2 1.4 1.4 7.2 6.5 Crude ®bre 7.3 6.7 ± ± 7.0 ± ± ± 6.0 8.3 5.5 10.0 8.3 5.3 5.9 8.0 7.2 6.6 10.0 9.4 16.1 16.8 ADF 10.7 10.6 10.7 11.0 10.7 9.0 12.2 ± ± ± ± ± ± ± 8.3 9.3 8.1 10.3 13.1 11.0 22.9 21.6 NDF 22.1 24.3 17.8 18.2 19.4 15.5 16.0 ± ± ± ± ± ± ± ± 15.6 14.6 14.7 20.2 14.3 26.9 25.8
Lignin 0.6 0.2 ± ± 0.4 ± ± ± ± ± ± ± ± 1.5 0.8 1.2 1.1 0.6 2.4 ± 2.8 0.9
Starch 44.2 ± ± ± 44.2 ± ± ± ± ± ± ± 41.2 ± ± 41.2 45.3 ± 40.0 ± 0.8 ±
Dry matter (% ar) ± 89.7 90.3 89.5 90.1 90.9 89.0 90.0 ± ± 90.0 87.6 91.9 ± 91.1 91.3 ± 90.2 ± 89.7 ± 91.1
aSource: (i) Abreu and Bruno-Soares (1998), (ii) Hanbury (unpublished), (iii) Aletor et al. (1994), (iv) Farhangi (1996), (v) Adsule et al. (1989), (vi) Infascelli et al.
(1995), (vii) Shobhana et al. (1976), (viii) Dhiman et al. (1983), (ix) Latif et al. (1975), (x) Urga et al. (1995), (xi) Kuo et al. (1995), (xii) Low et al. (1990), (xiii) Mean values from Petterson et al. (1997).
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contents, similar to ®eld pea and faba bean, conversely lupin has high fat and low starch content. The composition of the lipid fraction (Table 2) shows in most cases that the fatty acid pro®le is similar to other grain legumes, concentrations of stearic and linoleic acid are a little higher and oleic acid slightly lower. The data of Senatore and Basso (1994) differ from other data in bothL. cicera andL. sativus, they found levels of oleic acid considerably higher and levels of linoleic acid considerably lower than all other reports. Whether this difference is due to the methods of Senatore and Basso (1994) or a difference in the ItalianLathyrusecotypes examined is unclear, their results also differ from those for other grain legumes species (Table 2).
4.1.2. Mineral content
The data on L. ciceramineral content are more complete than those for L. sativus
(Table 3). Mineral contents of both species are similar and compare to other agriculturally important grain legumes. On the basis of the available data it does not appear that either species will be markedly different to the other grain legumes widely used.
4.1.3. Protein content and quality
The mean protein content inL. ciceraandL. sativusis 25 and 27%, respectively, from samples across a wide range of locations (Table 4). These are higher than protein contents in ®eld pea (23%) or faba bean (24%), but lower than in lupin (32%) (Petterson et al., 1997) or soybean (42%; Ravindran and Blair, 1992). Chandna and Matta (1994) found the composition of seed protein inL. sativus to be: albumins (14%), globulins (66%),
Table 2
Fatty acid composition ofL. ciceraandL. sativus(compared to ®eld pea (P. sativum), faba bean (V. faba) and
lupin (L. angustifolius))a
L. cicera L. sativus Field
pea
Faba bean
Lupin
i ii ii iii iv v vi vi vi
No. lines 2 2 3 1 1 1 5±16 3±8 3±174
Fatty acid(%of total fats)
Mystiric ± 0.4 0.6 ± 0.8 0.5 0.3 0.5 0.1
Palmitic 15.4 5.3 8.1 25 14.8 16.8 12.5 14.0 11.0
Palmitoleic ± 0.3 0.4 ± 0.3 ± ± ± 0.1
Stearic 7.9 18.7 13.8 2 7.5 4.6 1.2 2.3 3.7
Oleic 12.1 57.7 58.3 1 16.7 18.6 25.1 21.0 33.5
Linoleic 46.2 12.1 14.1 67 56.0 38.9 42.3 45.0 37.1
Non-adecanoic 0.8 ± ± ± ± ± ± ± ±
Linolenic 8.6 0.7 1.1 3 2.2 8.0 9.7 4.7 5.3
Arachidic 2.4 1.2 0.5 ± ± ± 0.7 1.8 0.9
Eicosadienoic 2.7 ± ± ± ± ± ± ± 0.4
Behenic ± 0.9 0.4 Trace ± ± 0.3 0.9 1.9
Total 96.1 97.3 97.3 98 98.3 87.4 91.8 89.3 92.1
aSource: (i) Hanbury (unpublished), (ii) Senatore and Basso (1994), (iii) Choudhury and Rahman (1973),
Table 3
Mineral content (as received) ofL. ciceraandL. sativus(includes comparison with ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a
L.cicera L. sativus Field pea Faba bean Lupin
i ii Mean ii iii iv v vi vii Mean viii viii viii
No. of lines 2 1 ± 1 1 25 1 1 3 ± 5±84 4±23 355±677
Mineral(mg/kg)
Se 0.12 ± 0.12 ± ± ± ± ± ± ± 0.07 0.05 0.08
Cu 7.6 5.6 6.9 8.2 ± ± ± 7.7 ± 8.0 4.8 10.3 4.9
Fe 70 78 73 38 ± 95 ± 63 74 89 53 77 75
Mn 11 12 12 15 ± ± ± ± ± 15 14 30 17
Zn 22 15 20 27 ± ± ± ± ± 27 30 28 35
B 9 14 11 11 ± ± ± ± ± 11 ± ± ±
Mineral(%)
P 0.30 0.27 0.29 0.34 0.31 0.44 0.26 0.32 0.41 0.42 0.34 0.41 0.30
K 0.88 0.86 0.87 ± ± ± ± 0.64 ± 0.64 0.91 0.96 0.81
Na 0.07 0.06 0.07 0.02 ± ± ± 0.04 ± 0.03 0.01 0.01 0.05
Ca 0.16 0.27 0.20 0.12 0.14 0.16 0.28 0.09 0.18 0.16 0.07 0.12 0.22
Mg 0.12 0.13 0.13 0.12 ± ± 0.11 0.09 ± 0.11 0.12 0.10 0.16
S 0.16 0.17 0.17 0.18 ± ± ± 0.14 ± 0.16 0.18 0.13 0.23
Ca:P 0.53 1.0 0.69 0.53 0.45 0.36 1.1 0.28 0.43 0.38 0.21 0.29 0.73
aSource: (i) Hanbury (unpublished), (ii) Farhangi (1996), (iii) Low et al. (1990), (iv) Urga et al. (1995), (v) Latif et al. (1975), (vi) Adsule et al. (1989), (vii)
Shobhana et al. (1976), (viii) Mean values from Petterson et al. (1997).
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glutelins (15%) and prolamins (5%); similarly; Duke (1981) also quotes values of 26, 53, 15 and 6%, respectively.
The amino acid pro®les of L. cicera and L. sativus (Table 5) are similar to those reported for many grain legumes (Petterson et al., 1997; Ravindran and Blair, 1992). For monogastric species most grain legumes are de®cient in the sulphur containing amino acids (methionine and cystine) but are rich in lysine (Gatel, 1994; Ravindran and Blair, 1992), this is also the case in L. cicera andL. sativus. In mixed diets, grain legumes, therefore, complement cereals, which have higher levels of methionine and cystine but lower levels of lysine. The mean lysine concentration inL. cicerais slightly lower than in
L. sativus, 6.16 (n3) cf. 6.8 g/16 g N (n12). Lysine contents per 16 g N are5% lower than in ®eld pea, and30% higher than in lupins (Table 5). On the basis of the protein composition bothLathyrusspp. have similar application to other legumes used as animal feed.
Little information is published onL. sativusandL. ciceraamino acid availabilities in monogastric and protein degradability in ruminant species. The protein degradability estimates from in sacco studies in three ruminant species (Table 6) showed bothL. sativus
andL. cicera to be similar to ®eld pea and faba bean. Protein degradabilities in both
Lathyrusspp. were usually slightly greater than lupin; and usually slightly less than in faba bean or ®eld pea.
4.1.4. Energy
For bothL. cicera andL. sativus, measures of energy are similar to those for many other common feed grain legumes. However,L. ciceraandL. sativushave consistently lower gross energy (GE) than lupin (which has a much higher fat content, Table 1) but are similar to ®eld pea and faba bean (Table 7).
Table 4
Protein concentrations (as received) reported inL. ciceraandL. sativus
Species Mean protein (%) No. lines Location Source
L. cicera 25 128 Spain Franco Jubete (1991)
26 51 ± Petterson et al. (1997)
23 20 Australia Laurence (1979)
24 17 Australia Hanbury (unpublished)
27 16 Syria Aletor et al. (1994)
L. sativus 24 114 Bangladesh Kaul et al. (1982)
28 76 Chile Tay et al. (2000)
29 41 ± Petterson et al. (1997)
26 40 Australia Laurence (1979)
31 36 Syria Aletor et al. (1994)
25 25 Ethiopia Urga et al. (1995)
30 15 India Ramanujam et al. (1980)
25 12 Australia Hanbury (unpublished)
25 10 Spain Franco Jubete (1991)
27 3 Canada Rotter et al. (1991)
Table 5
Amino acid concentrations (g/16 g N) and protein (as received) inL. ciceraandL. sativus(includes comparison with ®eld pea (P. sativum), faba bean (V. faba) and lupin
(L. angustifolius))a
L. cicera L. sativus Field pea Faba bean Lupin
i ii Mean ii iii iv v vi vii viii Mean ix ix ix
No. of lines 2 1 ± 1 1 3 1 4 1 1 ± 37 6 30
Amino acids(g/16 g N)
Cystine 1.26 ± 1.26 ± 1.39 1.53 ± 1.2 ± ± 1.4 1.49 1.37 1.48
Aspartic acid 9.54 11.81 10.30 10.45 11.8 ± 8.53 ± 14.6 9.97 11.07 10.16 10.53 9.29
Methionine 0.75 ± 0.75 ± 0.82 1.00 0.24 0.6 0.61 0.59 0.7 0.85 0.78 0.72
Threonine 3.31 3.99 3.54 3.55 4.08 4.04 2.59 2.6 5.15 3.82 3.5 3.35 3.54 3.36
Serine 4.58 4.95 4.70 4.75 4.73 ± ± ± 5.08 4.40 4.74 4.13 5.04 4.85
Glutamic acid 16.26 17.46 16.66 16.37 17.43 ± 13.40 ± 17.47 13.99 15.73 15.88 16.03 20.77
Proline 4.10 ± 4.10 ± 4.00 ± 3.07 ± 4.42 3.50 3.75 4.24 3.82 4.28
Glycine 3.74 4.00 3.83 3.43 4.20 ± 3.45 ± 3.91 3.91 3.78 4.13 4.20 4.12
Alanine 3.67 4.31 3.88 3.62 4.53 ± 3.20 ± 2.19 3.92 3.49 4.00 4.17 3.19
Valine 4.30 4.66 4.42 4.00 4.90 ± 3.91 4.4 5.08 5.88 4.6 4.29 4.30 3.91
Isoleucine 3.68 4.08 3.82 3.69 4.41 ± 3.41 5.0 4.82 3.89 4.5 3.89 3.80 3.97
Leucine 6.50 6.53 6.51 5.76 6.90 ± 5.93 6.6 8.60 6.42 6.7 6.54 7.27 6.61
Tyrosine 2.93 ± 2.93 ± 2.45 ± 2.39 ± 2.92 1.44 2.30 2.87 3.39 3.46
Phenylalanine 4.11 ± 4.11 ± 4.49 ± 3.26 4.2 3.89 2.95 3.9 4.17 4.12 3.65
Lysine 5.98 6.52 6.16 5.37 6.73 7.10 4.08 7.0 6.27 9.65 6.8 6.81 6.29 4.66
Histidine 2.18 ± 2.18 ± 2.61 ± 2.82 2.5 3.47 2.70 2.7 2.37 2.54 2.41
Arginine 7.90 7.96 7.92 7.28 8.04 ± 6.13 8.0 6.11 3.29 7.0 10.04 9.46 12.03
Protein (% ar) 26.8 23.6 25.7 26.8 24.5 26.9 27.4 ± 32.3b 25.6 27.2 23.0 24.1 32.2
aSource: (i) Hanbury (unpublished), (ii) Farhangi (1996), (iii) Low et al. (1990), (iv) Rotter et al. (1991), (v) Latif et al. (1975), (vi) Adsule et al. (1989), (vii) Kuo
et al. (1995), (viii) Ronda Lain et al. (1963), (ix) Mean values from Petterson et al. (1997).
bEstimated as 0.90% DM.
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Table 6
In sacco degradability parameters for protein and dry matter inL. ciceraandL. sativusgrain fed to ruminant
species (compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a
Animal Feed grain Parameter Degradability
Protein Cattleb L. cicera 0.53 0.46 0.36 0.93
Field pea 0.56 0.44 0.35 0.95
Faba bean 0.59 0.41 0.39 0.95
Lupin 0.51 0.50 0.22 0.92
Cattlec L. cicera 0.39 0.61 0.20 0.78
Field pea 0.52 0.48 0.18 0.87
Faba bean ± ± ± ±
Lupin 0.38 0.62 0.17 0.84
Buffalod L. sativus 0.52 0.48 0.17 0.88
Field pea ± ± ± ±
Faba bean 0.79 0.18 0.10 0.91
Lupin 0.34 0.66 0.17 0.84
Sheepd L. sativus 0.62 0.37 0.14 0.89
Field pea ± ± ± ±
Faba bean 0.70 0.28 0.11 0.89
Lupin 0.52 0.46 0.12 0.84
Dry matter Cattleb L. cicera 0.45 0.48 0.25 0.85
Field pea 0.50 0.49 0.22 0.90
Faba bean 0.47 0.46 0.29 0.86
Lupin 0.37 0.61 0.13 0.81
Cattlec L. cicera 0.34 0.62 0.16 0.72
Field pea 0.41 0.59 0.13 0.80
Faba bean ± ± ± ±
Lupin 0.33 0.67 0.14 0.80
Buffalod L. sativus 0.43 0.54 0.12 0.81
Field pea ± ± ± ±
Faba bean 0.6 0.34 0.09 0.82
Lupin 0.17 0.80 0.18 0.80
Sheepd L. sativus 0.59 0.37 0.07 0.81
Field pea ± ± ± ±
Faba bean 0.64 0.30 0.16 0.81
Lupin 0.14 0.83 0.14 0.75
aThe parameters describe the non-linear equation: fractional lossab 1ÿeÿct; t is the time (h).
Degradabi li ty i s determined at 0.05 fract i onal rumen out¯ow rate (r) according to:
degradabilityabc= cr, whereais the water soluble fraction,bthe potentially degradable fraction,c
the rate of loss ofbandtis the time (h).
bWhite (unpublished).
cGuedes and Dias da Silva (1996) incorporates a lag phase and is recalculated fromr0:044 tor0:05.
The metabolisable energy (ME) ofL. cicera may be slightly higher than L. sativus
(Table 8). The ME for both Lathyrus spp. in sheep are approximately 13 MJ/kg DM, similar to ®eld pea and faba bean. The sheep ME data of Farhangi (1996) are consistently lower than all other sources, the in vitro dry matter digestibility (DMD) method used to calculate ME is not recommended for grain (SCA, 1990). The single record for ME in cattle showsL. sativus to be similar to ®eld pea and faba bean (Table 8). In chickens,
Table 7
Gross energies (GE; MJ/kg as received) ofL. ciceraandL. sativuscompared to ®eld pea (P. sativum), faba bean
(V. faba) and lupin (L. angustifolius)
L. cicera L. sativus Field pea Faba bean Lupin Source
16.6a ± ± 17.0a ± Flores and Castanon (1991)
16.6a ± 16.6a 16.3a 18.1a Abreu and Bruno-Soares (1998)
16.7 16.9 17.1 16.7 18.4 Farhangi (1996)
16.2 16.7 16.6 16.7 18.3 Hughes (unpublished)
± 15.9 16.2 15.9 ± Duke (1981)
± 16.1 16.6 16.5 ± Guada Vallepuga (1972)
± 16.1 ± ± ± Low et al. (1990)
± ± 16.8 16.8 18.1 Petterson et al. (1997)
16.5 16.3 16.6 16.6 18.2 Mean
aEstimated as 0.90 MJ/kg DM.
Table 8
Metabolisable energy (ME), digestible energy (DE), available metabolisable energy (AME) and true
metabolisable energy (TME) of L. cicera and L. sativus, all in MJ/kg DM, for sheep, cattle and poultry
(compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a
Energy measure (MJ/kg DM)
Source L. cicera L. sativus Field pea Faba bean Lupin
ME sheep i 11.4 11.0 11.0 11.4 10.7
ii 14.2 ± ± ± 14.4
iii ± 14.0 13.9 13.3 ±
iv ± ± 12.0 11.5 12.2
v ± 14.4 13.1 13.7 ±
vi ± 12.9 11.8 12.3 ±
DE sheep vii 16.2 ± 16.5 16.3 16.5
v ± 17.5 15.8 16.7 ±
vi ± 15.8 14.2 15.0 ±
ME cattle and sheep viii ± ± 13.5 13.1 ±
ME cattle iii ± 12.9 12.7 12.7 ±
ME poultry ix ± 11.3 ± ± ±
AME poultry x 13.4 11.3 12.0 ± 7.9
iv ± ± 11.7 11.2 10.4
TME poultry xi 11.5 ± ± 12.5 ±
aSource: (i) Farhangi (1996), (ii) White (unpublished), (iii) Kearl (1982), (iv) Petterson et al. (1997), (v)
available ME is slightly higher in theLathyrusspp. than in lupin, but otherwise similar to ®eld pea and faba bean (Table 8).
4.1.5. Digestibility
Only a few studies have determined in vitro DMD and organic matter digestibilities (OMD). Similarly, little has been done on in vivo digestibilities. Generally, but not consistently, digestibilities ofL. cicera are slightly lower than for L. sativus. Both are, however, broadly similar to other commonly used grain legumes (Table 9). In vivo measures were usually higher than in vitro measures.
Several studies that have examined in sacco dry matter degradabilities have shown that
L. cicera and L. sativus have similar values to other commonly used grain legumes (Table 6). However, the parameters differ, particularly with lupin, which had a small water soluble fraction.
4.2. Antinutritional factors
In common with all grain legumes there are a range of antinutritional factors (ANFs) found in L. cicera andL. sativus grain. The ANFs commonly found in grain legumes include: tannins, phytic acid, oligosaccharides, protease inhibitors (trypsin and chymotrypsin inhibitors), amylase inhibitors and lectins (Liener, 1989). ODAP is also an ANF and is almost unique to theLathyrusgenus. There are only a small number of published studies of levels and activities of ANFs, other than ODAP, inL. sativus(Latif et al., 1975; Deshpande and Campbell, 1992; Aletor et al., 1994; Urga et al., 1995; Srivastava and Khokhar, 1996; Wang et al., 1998), and less onL. cicera(Aletor et al., 1994).
Table 9
In vitro dry matter digestibilities (DMD), in vitro organic matter digestibilities (OMD), in vivo DMD and in vivo
OMD in sheep ofL. ciceraandL. sativus(compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin
(L. angustifolius))a Digestibility measure (%)
Sourceb L. cicera L. sativus Field pea Faba bean Lupin
In vitro DMD i 82.1 ab 79.9 ab 82.7 a 80.3 ab 78.7 b
ii 88.6 a 92.9 b ± ± ±
In vitro OMD i 85.5 a 89.3 b 85.4 a 83.2 c 85.4 a
ii 85.5 a 90.3 b ± ± ±
In vivo DMD i 93.6 a ± ± ± 96.7 a
iii 93.0 a ± ± ± 95.5 a
iv ± 95.9 a 85.7 b 90.9 b ±
In vivo OMD iii 94.5 a ± ± ± 96.5 a
iv ± 95.6 a 86.9 b 91.8 ab ±
v 90.0 a ± 91.1 a 91.7 a 86.0 b
aWithin each row the values with different letters are signi®cantly different (P<0:05).
bSource: (i) Farhangi (1996), (ii) Aletor et al. (1994), (iii) White (unpublished), (iv) Zorita et al. (1972), (v)
4.2.1. Proteinaceous ANFs
The proteinaceous ANFs are (i) trypsin and chymotrypsin inhibitors (both protease inhibitors), respectively measured as trypsin inhibitor activity (TIA) and chymotrypsin inhibitor activity (CTIA), (ii) amylase inhibitors and (iii) lectins. ODAP will also be included under this heading, although ODAP is a non-protein amino acid and not strictly a proteinaceous ANF.
4.2.1.1. ODAP. Until recent times animal feeding studies withL. sativusorL. cicerahave been performed with no knowledge of the role of ODAP in lathyrism. Therefore, in all older studies of animal feeding (i.e. pre 1960s) the concentration of ODAP is unknown. Recent studies have shown that ODAP concentrations can vary widely both within and between the two species, however, environmental conditions are not as important as genotype (Hanbury et al., 1999). Nonetheless, stresses such as salinity and drought (Hussain et al., 1997) have been found to increase ODAP concentrations but are little understood. Generally L. cicera has lower seed ODAP concentrations than L. sativus
(Table 10). Concentrations of ODAP in the seed can be particularly high inL. sativusland races, up to 1.50% (Table 10).
1. TIA and CTIA
These inhibitors are destroyed in the rumen and so are not a problem for ruminant animals. In monogastric species they can result in hypertrophy of the pancreas if present in suf®cient quantities. There is often an increased production of S-containing enzymes which are lost due to forming indigestible complexes. Animal growth rate is commonly depressed by TIA and CTIA (Deshpande and Damodaran, 1990).
Due to different assay conditions, making comparisons between reported levels of TIA and CTIA (Table 11) are dif®cult. The reported ranges are lower inL. cicerathan
L. sativus (Aletor et al., 1994). Urga et al. (1995) claimed that measured TIA in
Table 10
ODAP content (% as received) mean and range of a number of lines ofL. ciceraandL. sativusgrown at various
locations
L. cicera L. sativus Location Source
Mean (range) No. Mean (Range) No.
0.15 (NA)a 128 0.20 (0.16±0.25) 10 Spain Franco Jubete (1991)
0.16 (0.10±0.22) 24 0.49 (0.07±0.75) 70 Syria Abd El-Moneim (1994)
0.13 (0.09±0.16) 16 0.49 (0.33±0.59) 36 Syria Aletor et al. (1994)
0.18 (0.08±0.34) 96 0.39 (0.04±0.76) 407 Australia Hanbury et al. (1999)
± ± 0.88 (0.45±1.40) 172 Bangladesh Kaul et al. (1982)
± ± 0.72 (0.37±1.04) 10 Ethiopia Tekle Haimanot et al. (1993)
± ± 0.44 (0.28±1.50) 1187 India Pandey et al. (1995)
± ± 0.32 (0.18±0.52) 76 Chile Tay et al. (2000)
± ± NA (0.08±0.99) 73 China Chen cited by Campbell (1997)
0.16 0.46 Grand mean
L. sativus (Table 11) was considerably lower than for soybeans, common beans and cowpeas, but higher than found in chickpeas, although the values in these species were not reported.
The TIA data can be compared to that of other feed legumes (measured by similar methods) to estimate a ranking for both L. cicera and L. sativus (Table 12). In summary, the species rank in likely order of increasing TIA: ®eld pea, faba bean,
L. cicera,L. sativus,P. vulgaris, soybean. Soybean is widely used for animal feeding but must be heated to destroy the protease inhibitors prior to feeding to monogastric animals.
2. Amylase inhibitor activity
Amylase is the enzyme primarily involved in starch digestion in mammals. Amylase inhibitors are thought to reduce amylase activity, but the extent to which they are important is debated (Deshpande and Damodaran, 1990). Deshpande and Campbell (1992) found in 100 lines ofL. sativus that the range of amylase inhibitor activity (AIA) was 3.6±91.4 units gÿ1 DM, substantially lower than the 330± 675 units gÿ1DM found inP. vulgariscultivars (Deshpande et al., 1982).
Table 11
Measured TIA and CTIA (units mgÿ1DM) ofL. ciceraandL. sativus
L. cicera No. lines L. sativus No. lines Source
TIA 12.6±20.4 16 20.1±44.1 36 Aletor et al. (1994)
9.15±15.1 2 ± Hanbury (unpublished)
± 16.7±26.2 25 Urga et al. (1995)
± 133±174 100 Deshpande and Campbell (1992)
CTIA 21±31 2 ± Hanbury (unpublished)
± 0±23 100 Deshpande and Campbell (1992)
Table 12
Relative comparisons (%) of measured TIA ofL. sativusandL. cicerain relation to ®eld pea (P. sativum), faba
bean (V. faba),Phaseolus vulgarisand soybean (G. max) (each relative comparison is made between similar
measurement techniques)a
Relative comparison Species TIA (%)
Field pea Faba bean L. cicera L. sativus P. vulgaris Soybean
1 ± ± ± 30 (i) 36 (i) 100 (i)
2 ± ± 32 (ii) 61 (ii) ± 100 (iii)
3 7 (iv) 18 (iv) ± ± 28 (iv) 100 (iv)
4 18 (v) 11 (v) ± ± 44 (v) 100 (v)
5 7 (vi) ± ± ± ± 100 (vi)
6 13 (vii) 5 (vii) 22 (viii) ± 100 (vii) ±
7 ± ± ± 56 (ix) 100 (x) ±
aSource: (i) Latif et al. (1975), (ii) Aletor et al. (1994), (iii) Smith et al. (1980), (iv) Deshpande and
3. Lectins
Lectins are present in most legumes (Liener, 1989), they interfere with nutrient digestion and absorption and increase wasteful protein synthesis, resulting in reduced ef®ciency of nutrient utilisation. Levels in L. cicera and L. sativus are unknown, however, Srivastava and Khokhar (1996) detected lectins in all of four lines of
L. sativus.
4.2.1.2. Proteinaceous ANF conclusions. Rotter et al. (1990) found that autoclaving feed containing 82%L. sativusincreased feed consumption and increased the efficiency of feed utilisation by chickens. In a separate sample autoclaving for 2 h decreased the concen-tration of ODAP from 0.24 to 0.11%. Such effects of heating are commonly known to occur for lectins, TIA and CTIA (Saini, 1989; Wiryawan and Dingle, 1999). Latif et al. (1975) found that heating could totally inhibit TIA inL. sativus. The extrusion ofL. sativus(which involves heating) before feeding to pigs removed any inhibitory effect on proteolytic activity, including trypsin activity, in pancreatic homogenates (Kapica et al., 1998).
The effect of various kinds of heating on the levels of ODAP are not clear. Boiling treatments seem to consistently reduce ODAP concentration by 30±90% (Tekle Haimanot et al., 1993; Srivastava and Khokhar, 1996; Padmajaprasad et al., 1997; Akalu et al., 1998). However, the effect of boiling is largely (though not wholly) due to the water solubility of ODAP. Roasting has been reported to both increase ODAP concentration (Tekle Haimanot et al., 1993) and to reduce it by 87% (Akalu et al., 1998). Akalu et al. (1998) found that heating induced isomerisation of b-ODAP (the neurotoxically active form) toa-ODAP (the benign form), however, there appeared to be an equilibrium of
60% of total ODAP in theb-ODAP form, irrespective of heating time. From the human nutrition perspective further research on reducing ODAP content during Lathyrusfood preparation is warranted. Given the variable results and the techniques required (possibly boiling) the pre-treatments are probably not practical for animal feeding purposes. The availability of low ODAP cultivars also reduces the need for such pre-treatment of animal feeds.
The results of heat treatment of L. sativus indicate that the protease inhibitors are inactivated as observed in other grain species. It would be desirable not to require heat treatment, however possible reductions in ODAP content could also occur. The presence of lines of negligible TIA indicates the potential for further reductions through breeding. There is insuf®cient data on the range of CTIA in eitherL. sativusorL. cicera, although with wider testing variation is highly likely to be found, given the variation present in other grain legume species. Such variation can be exploited in breeding programs.
4.2.2. Tannins
Tannins are polyphenolic compounds of two classes: low molecular weight hydrolysable and higher molecular weight non-hydrolysable (or condensed). It is postulated that condensed tannins bind to proteins in the digestive tract and form complexes which are frequently indigestible (Marquardt, 1989). The hydrolysable tannins are often found to have little effect on digestibility.
than lighter ones. Similarly, Deshpande and Campbell (1992) found that white or cream coloured seeds ofL. sativuswere associated with low tannin levels (both condensed and total), whereas seed with darker seed coats generally had high tannin levels. Similar observations regardingL. sativuswere made by Urga et al. (1995) and Wang et al. (1998). InL. sativus lighter seeds are associated with white ¯ower colour (Jackson and Yunus, 1984), consequently the selection of white ¯ower colour could be used to reduce tannin contents.
The range of condensed tannins in the literature is from undetectable to 0.77% (Table 13), with a smaller range inL. cicerathan inL. sativus. This may be a result of the smaller number of measurements and/or little selection of L. cicera in comparison to
L. sativuslines. UnlikeL. sativus, ¯ower colour inL. ciceradoes not vary greatly (Franco Jubete, 1991; Hanbury et al., 1995) and may be related to the small variation in tannin content. There is considerable scope for improvement of varieties with negligible condensed tannin levels. In the case ofL. sativus, much suitable germplasm is already identi®ed.
4.2.3. Phytate
Phytate is a cyclic compound that chelates with mineral ions (e.g. Ca, Mg, Zn, Fe) and forms compounds not readily absorbed in the intestine (Liener, 1989), thereby reducing animal performance. It is destroyed in the rumen and so is not a nutritional problem for ruminants. The range 0.49±1.09% in the two Lathyrus spp. (Table 14) is high in comparison to ®eld pea (0.15±0.70%) and faba bean (<0.01±1.04%; Petterson et al., 1997).
Table 13
Condensed tannins contents (catechin equivalents, % as received) inL. ciceraandL. sativus
Species Condensed tannins No. lines Source
Mean Range
L. cicera 0.36 0.27±0.55 16 Aletor et al. (1994)
0.68 0.59±0.77 2 Hanbury (unpublished)
L. sativus 0.12 0.00±0.44 100 Deshpande and Campbell (1992)
0.21 0.00±0.50 36 Aletor et al. (1994)
0.64 0.46±0.77 25 Urga et al. (1995)
0.31a 0.08±0.47a 9 Wang et al. (1998)
aEstimated as 0.90 of % DM.
Table 14
Phytate concentrations (% as received) inL. ciceraandL. sativus
Species Phytate (%) No. lines Source
Mean Range
L. cicera 0.80 0.80±0.81 2 Hanbury (unpublished)
L. sativus 0.71 0.49±0.96 25 Urga et al. (1995)
4.2.4. Oligosaccharides
Oligosaccharides are digested in the rumen but are indigestible to monogastric animals and lead to ¯atulence. High levels of oligosaccharides can impair nutrition and lead to distress and discomfort in animals. In two lines ofL. cicera, oligosaccharide levels were both 3.6% (Hanbury, unpublished), comparable to a range 3.0±4.8% in ®eld pea and 2.6±3.3% in faba bean (Petterson et al., 1997). Kuo et al. (1995) found oligosaccharide content in L. sativus to be 6.1% which they compared to faba bean with a mean of 3.4%.
4.2.5. ANF conclusions
The presence of ANFs is ubiquitous in grain legumes, consequently ANFs do not preclude the use of L. ciceraand L. sativus as feed grain. However, improvement on cultivars is desirable and, on the basis of variation that exists in the germplasm, there is considerable scope for rapid improvement. Total reduction of ANFs may not be desirable as they can also function as protection against disease and pest attack.
In the case of trypsin inhibitors, chymotrypsin inhibitors, tannins and phytate in L. ciceraandL. sativusvariation within the germplasm is already available, or likely to be available on the basis of known variation among other grain legume species. This indicates that substantial improvements inL. ciceraandL. sativuscultivars can be made. Most of the ANFs, other than ODAP, currently identi®ed are in quantities less than those already encountered in other common grain legumes and are consequently unlikely to cause any serious concerns when used as animal feeds. Heating may be used to reduce the level of proteinaceous ANFs and ODAP. The degree that this is necessary needs to be determined by feeding studies. It is highly likely that improvements in cultivars will lessen any need for heat treatments.
4.3. Animal feeding studies
4.3.1. General
As for human food there are many historical references to the use ofLathyrusspp. as animal feed or fodder, principallyL. sativus,L. cicera,L. ochrusandL. clymenum. Use of
L. sativus and L. cicera is referred to by Columella in the ®rst century A.D.
(PenÄa-Chocarro and Zapata PenÄa, 1999).
Because of concerns of human lathyrism there has been an emphasis in many countries to develop L. sativus cultivars with lower ODAP levels (Roy et al., 1993; Campbell et al., 1994) with some success. Consequently, recent animal feeding studies have been able to both quantify the amount of ODAP in the diet and provide a low ODAP intake at higher inclusion rates ofL. sativus. Few studies ofL. ciceraas animal feed have been conducted. Due to the possible high variability in ODAP content in the lines used in older studies their results should be interpreted cautiously. Lathyrism can occur in both monogastrics and ruminants. Whether this can be avoided in low ODAP Lathyrus
spp. lines and what constitutes a safe dose of ODAP in any species of animal is not certain.
be able to degrade ODAP. Horses are noted as being very susceptible to lathyrism with symptoms of paralysis of the hind limbs and sometimes dying, following heavy grazing or feeding onLathyrusspp. seed (Stockman, 1932; Steyn, 1933; LoÂpez Bellido, 1994). There is anecdotal evidence of pigs, sheep and cattle having died due to lathyrism after being turned intoLathyrus spp. ®elds (Stockman, 1932). He also claims that pigs may thrive on a pure diet ofLathyrusspp. seed, despite developing weakness in the hind legs. Monkeys can be affected similarly to humans by consumption of L. sativus and death sometimes results (Rao et al., 1967). It is reported that many species of birds are readily affected by lathyrism when consuming Lathyrusspp. seed (Stockman, 1932), although Franco Jubete (1991) reported that in Spain doves fed avidly onL. cicerawith no obvious ill-effects. Lewis et al. (1948) fedL. sativusandL. cicerato young rats at 50% of food intake for 7±21 weeks and did not induce any lathyritic symptoms, growth rates were similar to those fed a diet based on ®eld peas. Basu et al. (1937) found no lathyrism symptoms in rats fed 15%L. sativusfor 8 weeks, growth rates were lower than those fed ®eld peas.
According to reports from Spain (LoÂpez Bellido, 1994) occasional consumption of
L. sativusorL. ciceragrain does not harm horses or sheep. In small areas of Spain, where these species are still cultivated both L. sativus and L. cicera grain is fed to stock, sometimes with the exception of pigs (PenÄa-Chocarro and Zapata PenÄa, 1999). In sheep bothL. sativusandL. ciceragrain are often used for gestating females, fattening lambs and serving males;L. cicera can be included at up to 50% of the feed ration with no symptoms of lathyrism (LoÂpez Bellido, 1994). Up to 350 g ofL. ciceraseed per day is fed to lactating ewes by Spanish shepherds without harmful effects (Franco Jubete, 1991). Tekle Haimanot et al. (1997) reported that in a small study most horses, donkeys, goats and sheep developed spasticity in the hind limbs after 1±3 years feeding onL. sativus
grain. They noted that the new born goats and sheep were quite sensitive to lathyrism, the symptoms being evident after 1±3 months. Cattle producers in northern Spain have used
L. ciceragrain widely, with the peak area of production 24 000 ha in 1983±1986 (Franco Jubete, 1991).
Although levels of ODAP were not reported in the above mentioned studies, evidence exists indicating that rumen micro¯ora adapt to ODAP and break it down. Bacteria have been isolated from soil sludge which can use ODAP as their sole carbon and nitrogen source (Yadav et al., 1992). In sheep, tolerance toL. sylvestrisin their diet seems due to changes in the rumen contents (Rasmussen et al., 1992), presumably increasing breakdown of DABA, a neurotoxin chemically similar to ODAP (Fig. 1). Fermenting
L. sativusseeds withAspergillus oryzaeandRhizopus oligosporusfor 48 h each has been shown to reduce ODAP concentration by >90% (Kuo et al., 1995). Farhangi (1996) incubated L. sativus and L. cicera grain in sheep rumen ¯uid and reported a rapid disappearance of ODAP (>90% in 4 h), supporting the idea that certain rumen micro-organisms can destroy the toxin.
4.3.2. Chickens
Low et al. (1990) found that inclusion of low ODAPL. sativusgrain at 82% of the diet for up to 4 weeks (commenced at age 7 days) did not induce any symptoms of lathyrism in chickens. Control chickens fed a wheat/soybean based diet grew more rapidly. The ODAP concentration in the seed used was not measured, although the line was known to have low levels (mean 0.13%), low variation within a line is consistent in bothL. sativus
andL. cicera (30%; Hanbury et al., 1999).
Rotter et al. (1991) fed high (0.27%), medium (0.22%) and low (0.13%) ODAP lines of
L. sativusto chickens at 20±80% of the diet. They found that an increased proportion of
L. sativus seed in the diet of young chickens decreased weight gain, feed intake and ef®ciencies of feed conversion (feeding commenced at age 7 days). At 20 and 40% proportions there were minor or no differences to a wheat/soybean diet. However, using 0.27% ODAP seed generally resulted in decreased weight gain, feed intake and ef®ciencies of feed conversion, compared to lower ODAP seed. Since increasing the proportion ofL. sativus above 40% (irrespective of ODAP concentration) also affected the chickens it can be concluded that there were ANFs in the seed (other than ODAP) which were not characterised.
4.3.3. Pigs
Castell et al. (1994) fed starter pigs (15±35 kg liveweight) high ODAP (0.30% in the seed)L. sativusat up to 40% of the feed ration. The increased inclusion rate ofL. sativus
reduced average daily weight gain (ADG) by up to 25%, decreased ef®ciency of feed conversion by up to 10% and reduced voluntary feed intake (VFI) by up to 19% in linear dose responses. Heart and spleen weights as a proportion of liveweight were also signi®cantly reduced by the increased level ofL. sativus. Castell et al. (1994) also fed
L. sativusto grower-®nisher pigs (25±100 kg liveweight) and reported a signi®cant linear reduction in ADG and VFI with increasing proportion ofL. sativus(up to 30% of intake). In two experiments, both high (0.27%) and low (0.09%) ODAP lines were used, and it was found that increased concentration of ODAP signi®cantly reduced ADG and VFI independently of the inclusion rate of L. sativus in the diet. There was a signi®cant linear effect of increased L. sativus inclusion rate on increases in liver and kidney weight relative to liveweight, differing from observations in starter pigs. Scores for visual appeal of meat fell slightly with increased inclusion rates. Following slaughter no evidence could be seen of degeneration of the spinal cord or nerve tissue indicative of neurolathyrism. No trace of ODAP could be found in loin samples at a detection level of 100 ng gÿ1. It can be concluded from this work that increased ODAP concentration (as varied by concentration of ODAP in L. sativus) probably reduced pig performance. However, other ANFs may possibly have been at higher levels in the higher ODAPL. sativus. The inclusion rate of L. sativushad a much greater effect than ODAP level, implying that ANFs other than ODAP were more important in reducing growth rates.
(FCR) at any substitution rate. Liver and kidney weights were also unaffected. No indications of lathyrism were observed. Weaner pigs (5±13 kg liveweight) showed no signs of lathyrism and no difference in ADG, VFI and FCR to controls, when fed
L. cicera (0.10% ODAP) at up to 15% of their diet (Mullan, unpublished). When fed L. cicera at 20% of the diet ADG was 10% lower with similar increases in FCR, probably due to the high levels of plant protein in their immature digestive systems.
4.3.4. Sheep
Farhangi (1996) compared effects of whole L. cicera grain (0.17% ODAP) to lupin (Lupinus angustifolius) grain in two experiments with sheep. In experiment 1, 12 mature Merino wethers were fed diets containing 15% either wholeL. ciceraor lupin grain for 17 days. No signs of toxicity were observed and there were no differences in VFI due to the treatments. In experiment 2, a total of eight immature Merino wethers were fed diets of 25% L. cicera or lupin for 73 days. No gross signs of neurolathyrism were reported. However, feed intake and growth rate were reduced by 7 and 30%, respectively, and wool growth by 19% in sheep fed the L. cicera diet. The small number of sheep in the experiments was a problem in obtaining signi®cant results, and only the wool growth differences were statistically signi®cant (P<0:05) in experiment 2.
White (unpublished) compared immature Merino wethers fed L. cicera cv. Chalus (0.10% ODAP) or lupin, ad libitum over a 10-week period.L. ciceraand lupin were fed at two rates, 35 and 70% of the diet, the remainder being hay. There were 20 sheep per diet group, fed individually. The sheep fedL. cicerashowed greater liveweight gains, dressed carcass weights, VFI and ef®ciencies of feed conversion than those fed lupins. Ef®ciencies of feed conversion for 35 and 70% lupin diets were 10.6 and 11.5, respectively, and for 35 and 70%L. ciceradiets were 11.6 and 13.2%, respectively. There were no indications of animal ill health in behaviour, carcasses or biochemical analyses conducted throughout the experiment. Quality testing of meat showed equal or better results forL. cicerathan lupins and wool growth was similar for all diets. Overall, the results indicated that sheep fed theL. cicera diets performed better than those fed the lupin diets.
5. Conclusions
5.1. Animal feeding conclusions
The pig feeding studies indicate that grain of Lathyrus spp. of low ODAP concentrations can be fed at 30% of the diet without any effect on animal performance. However,L. sativusmay have higher levels of ANFs (possibly TIA and CTIA, Table 11) since similar inclusion rates at the same ODAP concentration (0.09%) reduced growth rates usingL. sativus(Castell et al., 1994) but not usingL. cicera(Mullan et al., 1999). Younger pigs do not perform optimally if fed more than 15%L. cicera(0.09% ODAP), but this is probably due to sensitivity to plant protein, not to ODAP.
signi®cant effects of ANFs other than ODAP. There are no data on poultry performance usingL. cicera.
Both pigs and poultry showed depressed performance when high ODAP (0.27%)
L. sativusline were fed. Whether this was due to ODAP or other ANFs in the Canadian varieties used is unclear. Further characterisation of the ANFs in both L. sativus and
L. cicerais necessary to separate the effects of ODAP from those of other ANFs. Until this is performed higher ODAP lines (0.15% or higher) should be avoided.
Sheep, and presumably other ruminants, can tolerate high levels of inclusion (up to 70% of 0.09% ODAP L. cicera) with no reduction in performance. ODAP and other ANFs are probably broken down in the rumen. It is unlikely that ANFs other than ODAP in any lines ofL. sativusandL. cicerawill signi®cantly affect ruminants. Since a 70% inclusion rate is unlikely to be used in practical ruminant feeding higher ODAP varieties could certainly be tolerated at inclusion rates below 70% (i.e. in this case if the intake of ODAP does not exceed 0.063% of the diet in sheep of 35±48 kg liveweight).
Caution should be taken when usingL. ciceraorL. sativusin the diet of young animals because they are thought to be more susceptible to ODAP than older animals. However, the evidence for this is inconclusive, and needs to be veri®ed by experiment. Young pigs can tolerate low ODAP (0.09%)L. ciceraat rates (up to 15% of diet) used for other grain legumes, but they may not be tolerant to higher levels of ODAP. Further comparisons betweenLathyrusspp. and other grain legumes considered safe (e.g. ®eld peas) need to be performed using young animals.
5.2. General conclusions
The serious consequences of lathyrism for animals means that caution must be exercised in feeding recommendations. There is suf®cient evidence to justify the conclusion that safe feeding levels (summarised in Section 5.1) over extended periods are possible with the reduced ODAP levels of cultivars and germplasm now available. However, reduction in animal growth rates due to both ODAP and other ANFs have been recorded. Similarly to other commonly used grain legumes, the heating ofL. ciceraand
L. sativus will reduce the level and activities of the proteinaceous ANFs, which are particularly important for the monogastric species, also with possible reductions in ODAP content. Little improvement in ANFs (other than ODAP) has been attempted in breeding of eitherL. ciceraorL. sativus. The improvement of cultivars is possible in a short time frame, given the variation already recorded and available to breeding programs, particularly inL. sativus. Experience with other species of grain legumes indicates that variation in the known ANFs will be present in the germplasm. The germplasm for both
Lathyrus species is large, to date relatively unutilised and, particularly for L. sativus, highly variable.
Compositions of bothL. ciceraandL. sativusare generally similar to ®eld pea; apart from the presence of ODAP, and their generally higher protein and ANF levels. Feeding data already shows that current cultivars can perform as well as industry standard ingredients. This indicates that rapid exploitation of these species in the feed industry is possible given experimentally established feeding recommendations. Since both
Mediterranean-type environments the potential of a rapidly developed market for grain would be one incentive for growers in these areas to adopt these crop options, particularly for those attempting to replace pasture legume rotations with low input grain legume crops.
Acknowledgements
We would like to thank Mr. Bob Hughes and Mr. Peter Zviedrans, South Australian Research and Development Institute and Mr. Miyan Shahajahan, University of Adelaide for GE and AME data. We would also like to thank the Grains Research and Development Corporation, CLIMA, Agriculture Western Australia and CSIRO, Division of Animal Production for providing funds and facilities.
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