Review article
A review of the potential of Lathyrus sativusL. and L. cicera L. grain for use as animal feed
C.D. Hanburya,*, C.L. Whiteb, B.P. Mullanc, K.H.M. Siddiquea,c
aCentre for Legumes in Mediterranean Agriculture (CLIMA), University of Western Australia,
Nedlands 6907, AustraliabCSIRO, 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 cicera and L. sativus, as grain legumes for
human and animal consumption, dates to the Neolithic period. Due to its tolerance to harsh
environmental conditions L. sativus is still used widely for human food in Ethiopia and the Indian
sub-continent, although cultivation has diminished in many other regions.
The grain of both L. cicera and 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 of L. cicera or L. sativus can 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 both L. cicera and L. sativus are similar to other commonly used feed grain
legumes, respective protein contents are 25 and 27%. Antinutritional factors (ANFs), other than
ODAP, are present in both L. cicera and L. sativus at 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 in L. cicera and L. sativus on 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 of L. cicera and L. sativus has 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
Animal Feed Science and Technology
87 (2000) 1±27
* 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.
PII: S 0 3 7 7 - 8 4 0 1 ( 0 0 ) 0 0 1 8 6 - 3
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, both L. 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
Lathyrus spp., 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).
It has been demonstrated in recent studies that two Lathyrus spp. (L. sativus L. and L.
cicera L.) have considerable potential as grain legume crops on ®ne textured, neutral to
alkaline, soil types in southern Australian Mediterranean-type environments (Hanbury
et al., 1995; Siddique et al., 1996, 1999; Siddique and Hanbury, 1998). In Australia the
adaptation of the two species is slightly different, L. cicera seeming better adapted to
lower rainfall (250±350 mm annually) regions and L. sativus to medium rainfall (350±
600 mm annually). They are being evaluated as low input, multi-purpose crops for green
manuring, animal feed and fodder. In Australia, animal feed is seen as the primary use of
the grain of these species, both on and off farm. Animal feeding with both species has a
long history and is still practised in some parts of the world. However, published studies
are scattered and frequently dif®cult to access. This review aims to summarise the animal
feeding literature and demonstrate the potential for the two species as animal feed.
2 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
The genus Lathyrus is 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 related L. sativus (grass pea) and L.
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 both L. sativus and L. cicera were cultivated on the
Iberian peninsula in the Neolithic period (PenÄa-Chocarro and Zapata PenÄa, 1999).
Evidence also suggests that L. 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
that L. sativus was originally domesticated as a secondary crop as a result of being a weed
of lentil (Lens culinaris) crops.
2. Lathyrism
Lathyrus species, particularly L. 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. pusillus and L. 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 be b-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 either L. sativus or L. cicera (Bell, 1962, 1964), there is evidence that a
BAPN precursor (2-cyanoethyl-isoxazolin-5-one) is present in L. sativus seedlings 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 of L. sativus or L. 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 different Lathyrus species and some Vicia species. The symptoms
are weakness of the hind limbs and paralysis or rigidity of the muscles. Within the
Lathyrus genus, the category of neurolathyrism has been further divided into two sub-
categories. One is caused by the compound L-2,4-diaminobutyric acid (DABA; Fig. 1),
primarily in the perennial species L. sylvestris (Foster, 1990) and L. latifolius (Barrow
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 3
et al., 1974). However, DABA is not found in L. cicera or 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 as b-N-oxalylamino-L-alanine or BOAA; Fig. 1): which has been recorded
in humans and animals following consumption of L. sativus, L. cicera, L. ochrus and L.
clymenum (Barrow et al., 1974; Padmanaban, 1980; Franco Jubete, 1991). The seed of a
number of other uncultivated Lathyrus species have been found to contain ODAP (Bell,
1962, 1964). Historically the consumption of L. sativus has been most often linked with
lathyrism in humans and animals, primarily because of all Lathyrus species 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
upon L. 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 of L. 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 of b-aminopropionitrile (BAPN), L-2,4-diaminobutyric acid (DABA), 3-(-N-oxalyl)-L-2,3-diamino propionic acid (ODAP or BOAA) and glutamate.
4 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
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 0.11 mmol gÿ1 ODAP 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 of Lathyrus for 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
The proximate compositions of L. cicera and L. sativus are generally very similar to
®eld pea and faba bean (Table 1). Both Lathyrus spp. have low fat and high starch
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 5
Table 1
Composition of L. cicera and L. sativus in 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
a Source: (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 both L. cicera and L. 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 Italian Lathyrus ecotypes 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. cicera mineral 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 in L. cicera and L. sativus is 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 in L. sativus to be: albumins (14%), globulins (66%),
Table 2
Fatty acid composition of L. cicera and L. 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
a Source: (i) Hanbury (unpublished), (ii) Senatore and Basso (1994), (iii) Choudhury and Rahman (1973),
(iv) Kuo et al. (1995), (v) Grela and GuÈnter (1995), (vi) Mean values from Petterson et al. (1997).
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 7
Table 3
Mineral content (as received) of L. cicera and L. 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
a Source: (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 and L. 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 in L. cicera is slightly lower than in
L. sativus, 6.16 (n � 3) cf. 6.8 g/16 g N (n � 12). Lysine contents per 16 g N are �5%
lower than in ®eld pea, and �30% higher than in lupins (Table 5). On the basis of the
protein composition both Lathyrus spp. have similar application to other legumes used as
animal feed.
Little information is published on L. sativus and L. cicera amino 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 both L. sativus
and L. cicera to be similar to ®eld pea and faba bean. Protein degradabilities in both
Lathyrus spp. were usually slightly greater than lupin; and usually slightly less than in
faba bean or ®eld pea.
4.1.4. Energy
For both L. cicera and L. sativus, measures of energy are similar to those for many
other common feed grain legumes. However, L. cicera and L. sativus have 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 in L. cicera and L. 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)
29 3 India Shobhana et al. (1976)
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 9
Table 5
Amino acid concentrations (g/16 g N) and protein (as received) in L. cicera and L. 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
a Source: (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).b Estimated as 0.90% DM.
10
C.D
.H
an
bury
eta
l./An
ima
lF
eedS
cience
an
dTech
nolo
gy
87
(2000)
1±27
Table 6
In sacco degradability parameters for protein and dry matter in L. cicera and L. sativus grain fed to ruminant
species (compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a
Animal Feed grain Parameter Degradability
(at r � 0:05)Soluble
fraction (a)
Potentially
degradable
fraction (b)
Rate of
degradation
(c)
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
a The parameters describe the non-linear equation: fractional loss � a� b�1ÿ eÿct�; t is the time (h).
Degradabili ty is determined at 0.05 fract ional rumen out¯ow rate (r) according to:
degradability � a� bc=�c� r�, where a is the water soluble fraction, b the potentially degradable fraction, c
the rate of loss of b and t is the time (h).b White (unpublished).c Guedes and Dias da Silva (1996) incorporates a lag phase and is recalculated from r � 0:044 to r � 0:05.d Infascelli et al. (1995).
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 11
The metabolisable energy (ME) of L. 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 shows L. sativus to be similar to ®eld pea and faba bean (Table 8). In chickens,
Table 7
Gross energies (GE; MJ/kg as received) of L. cicera and L. sativus compared 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
a Estimated 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 ±
a Source: (i) Farhangi (1996), (ii) White (unpublished), (iii) Kearl (1982), (iv) Petterson et al. (1997), (v)
Guada Vallepuga (1972), (vi) Zorita et al. (1972), (vii) Abreu and Bruno-Soares (1998), (viii) ARFC (1993), (ix)
Latif et al. (1975), (x) R.J. Hughes, personal communication, (xi) Flores and Castanon (1991).
12 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
available ME is slightly higher in the Lathyrus spp. 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 of L. 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 and L. 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 the Lathyrus genus. There are only a small number of
published studies of levels and activities of ANFs, other than ODAP, in L. 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 on L. 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 of L. cicera and L. 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
a Within each row the values with different letters are signi®cantly different (P < 0:05).b Source: (i) Farhangi (1996), (ii) Aletor et al. (1994), (iii) White (unpublished), (iv) Zorita et al. (1972), (v)
Abreu and Bruno-Soares (1998).
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 13
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 with L. sativus or L. cicera have
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 in L. sativus land
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 in L. cicera than
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 of L. cicera and L. sativus grown 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
a Not available.
14 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
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 of L. sativus that the range of amylase inhibitor
activity (AIA) was 3.6±91.4 units gÿ1 DM, substantially lower than the 330±
675 units gÿ1 DM found in P. vulgaris cultivars (Deshpande et al., 1982).
Table 11
Measured TIA and CTIA (units mgÿ1 DM) of L. cicera and L. 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 of L. sativus and L. cicera in relation to ®eld pea (P. sativum), faba
bean (V. faba), Phaseolus vulgaris and 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) ±
a Source: (i) Latif et al. (1975), (ii) Aletor et al. (1994), (iii) Smith et al. (1980), (iv) Deshpande and
Damodaran (1990), (v) Elkowicz and Sosulki (1982), (vi) Saini (1989), (vii) Petterson et al. (1997), (viii)
Hanbury (unpublished), (ix) Deshpande and Campbell (1992), (x) Deshpande et al. (1982).
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 15
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. sativus increased 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 in L. sativus. The extrusion of L. 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) to a-ODAP (the benign form), however, there appeared to be an equilibrium of
�60% of total ODAP in the b-ODAP form, irrespective of heating time. From the human
nutrition perspective further research on reducing ODAP content during Lathyrus food
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 either L. sativus or L. 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.
Tannins in faba beans and ®eld peas are frequently localised in the seed coat
(Marquardt, 1989; Gatel and Grosjean, 1990), with high tannin levels in darker seed coats
16 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
than lighter ones. Similarly, Deshpande and Campbell (1992) found that white or cream
coloured seeds of L. sativus were associated with low tannin levels (both condensed and
total), whereas seed with darker seed coats generally had high tannin levels. Similar
observations regarding L. sativus were made by Urga et al. (1995) and Wang et al. (1998).
In L. 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 in L. cicera than in L. sativus. This may be a result of the
smaller number of measurements and/or little selection of L. cicera in comparison to
L. sativus lines. Unlike L. sativus, ¯ower colour in L. cicera does 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 of L. 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) in L. cicera and L. 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)
a Estimated as 0.90 of % DM.
Table 14
Phytate concentrations (% as received) in L. cicera and L. 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)
1.07 1.03±1.09 4 Srivastava and Khokhar (1996)
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 17
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 of L. 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. cicera and 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.
cicera and L. sativus variation 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 in L. cicera and L. sativus cultivars 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 of Lathyrus spp. as
animal feed or fodder, principally L. sativus, L. cicera, L. ochrus and L. 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 of L. sativus. Few studies of L. cicera as 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.
Observations on the effects on different animal species when fed on Lathyrus spp. of
unknown ODAP content differ. There is some evidence that rumen micro-organisms may
18 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
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 on Lathyrus spp. 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 into Lathyrus spp. ®elds (Stockman, 1932). He also claims that pigs may
thrive on a pure diet of Lathyrus spp. 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 Lathyrus spp. seed (Stockman, 1932), although
Franco Jubete (1991) reported that in Spain doves fed avidly on L. cicera with no obvious
ill-effects. Lewis et al. (1948) fed L. sativus and L. cicera to 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. sativus for 8 weeks, growth rates were lower than those fed
®eld peas.
According to reports from Spain (LoÂpez Bellido, 1994) occasional consumption of
L. sativus or L. cicera grain 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
both L. sativus and L. cicera grain 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 of L. cicera seed 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 on L. 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. cicera grain 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 to L. sylvestris in 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. sativus seeds with Aspergillus oryzae and Rhizopus oligosporus for 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.
There are only a small number of feeding studies in which ODAP levels have been
measured or estimated, and each of these will be discussed. Using L. sativus lines of seed
with a ODAP content of �0.08%, no symptoms of lathyrism were observed in donkeys,
pigs or sheep when fed as 50±80% of daily intake for 180±250 days (Chen referred by
Campbell, 1997); details are not available.
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 19
4.3.2. Chickens
Low et al. (1990) found that inclusion of low ODAP L. sativus grain 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 both L. sativus
and L. 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. sativus to 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 of L. 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. sativus at up to 40% of the feed ration. The increased inclusion rate of L. 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 of L. sativus. Castell et al. (1994) also fed
L. sativus to grower-®nisher pigs (25±100 kg liveweight) and reported a signi®cant linear
reduction in ADG and VFI with increasing proportion of L. 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 ODAP L. sativus. The inclusion rate of L. sativus had a much greater effect
than ODAP level, implying that ANFs other than ODAP were more important in reducing
growth rates.
In contrast with the results of Castell et al. (1994) using L. sativus, Mullan et al. (1999)
fed L. cicera (0.09% ODAP) to pigs from 15 to 110 kg liveweight at substitution rates up
to 30% of the diet, diets were matched for sulphur amino acids. In comparison to the
standard soybean based diet there was no difference in ADG, VFI or feed conversion ratio
20 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
(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 whole L. cicera or 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. cicera and 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 fed L. cicera showed 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. cicera diets 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 for L. cicera than lupins and wool growth was similar for all diets. Overall, the
results indicated that sheep fed the L. 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. sativus may 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 using L. sativus (Castell et al., 1994) but not using L. 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.
Poultry seem able to tolerate up to 40% of their diet of L. sativus of moderate ODAP
concentrations (0.27%) with minor reductions in growth. Above 40% there appears to be
C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 21
signi®cant effects of ANFs other than ODAP. There are no data on poultry performance
using L. cicera.
Both pigs and poultry showed depressed performance when high ODAP (0.27%)
L. sativus line 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. cicera is 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 of L. sativus and L. cicera will 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 using L. cicera or L. sativus in 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. cicera at rates (up to 15% of diet) used for other grain
legumes, but they may not be tolerant to higher levels of ODAP. Further comparisons
between Lathyrus spp. 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 of L. cicera and
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 either L. cicera or L. sativus. The improvement of cultivars is possible in a short time
frame, given the variation already recorded and available to breeding programs,
particularly in L. 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 both L. cicera and L. sativus are 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
L. sativus and L. cicera are well adapted to large areas of southern Australia and other
22 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27
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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