The toxicity of Vicia species and their utilisation as grain legumes
Dirk Enneking B.Ag.Sc. PhD Ag.Sc. (Adelaide)
Veni, Vidi: Vicia
The worldwide utilisation of Vicia species as forage and green manure crops is well established. Except for V. faba L., the utilisation of Vicia species as grain legumes is of minor global economic importance and mainly restricted to the Mediterranean region and South-West Asia, where the grain is used primarily as seed and in ruminant diets.
In Australia, the comparatively high seed yields and low production costs for genotypes from species such as V. narbonensis L. (narbon bean or moor's pea) and V. sativa L. (common vetch) have provided an attractive alternative grain legume option for dryland farming and have thus stimulated an interest in markets for the grain. Monogastric animals ( incl. humans) are the major global end-users for grain legume products. Because of the well known toxicity of Vicia spp. seeds to mono gastric animals in particular, this thesis has focussed on those major toxic chemical seed components which are perceived as major constraints to the wider utilisation of these promising crops as grain legumes. A thorough examination of current and past practices of vetch cultivation and utilisation was undertaken to complement this approach.
The two major aims were, first to elucidate the nature of the factors responsible for the low palatability of narbon beans to pigs, and second to review the available information about the toxicity of Vicia species and their utilisation as grain legumes.
The potent feed inhibitory activity of Namoi vetch (V. villosa Roth cv. Namoi) provided a useful model for the initial stage of this study. Its antifeedant activity was shown to be due to the toxic amino acid canavanine. Inclusion of canavanine in pig diets at a concentration equivalent to that found in Namoi vetch seed accounted fully for the feed inhibitory activity of this legume. The novel effect of this well known arginine analogue may well be explicable in terms of the inhibition of the arginine pathway leading to nitric oxide which is now known to be involved in the control of peristalsis.
The experience gained with Namoi vetch in the feed-intake bioassay proved to be invaluable for the isolation of the much less potent -glutamyl-S-ethenyl-cysteine feed inhibitor from the narbon bean. A quantitative assessment of this factor's feed inhibitory activity was not permitted due to the untimely death of our veterinary colleague, Dr. Richard Davies. There is, however, a clear correlation between the total S-ethenyl cysteine content of the tested diets and the negative porcine feed intake responses.
An important difference between V. villosa and V. narbonensis was noted, as demonstrated by the rate at which the pigs reduced their feed intake. It is remarkable, that the effect of canavanine-containing diets becomes evident only after the second meal, whereas the pigs immediately restrict their feed intake when presented with diets containing S-ethenyl-cysteine. Such a clear delineation of feed-intake responses provides a simple and general classification for feed-intake inhibitors, and may be worthy of further detailed physiological studies. The antifeedant effects of these compounds suggest that they have evolved as part of the plants' anti-predator defence strategy.
Particular attention, including a detailed review of its economic botany, has been given to V. narbonensis, a relatively unknown but promising grain crop for Australia. With the chemical identity of the unpalatability established, the selection of more palatable genotypes is likely to provide access for the grain to monogastric feed markets. The historical evidence suggests that V. narbonensis is a niche crop of particular value for specific agricultural applications, its conversion into a broad acre crop is a challenge for the future.
V. sativa was investigated as a direct consequence of a request to chemically examine the toxin content of the cultivar Blanche Fleur. By the time that investigation commenced, Blanche Fleur, which was originally introduced to Australia as a hay, forage and green manure crop, had already been prematurely promoted and exported as acheap replacement for red lentils (Lens culinaris Med.) in ignorance of this species' well documented content of -glutamyl--cyanoalanine and the favism toxin, vicine. A 1992 commentary article to Nature (Tate, M. E. and Enneking, D. (1992) A mess of red pottage. Nature 359, 357-358) onour observations led to a ban on its importation by India and Egypt. Subsequent poultry bioassays established that the cyano-alanine content was substantially altered by cooking to produce some as yet un-identified nitrile component, but the feed inhibitory activity of the cooked grain was undiminished. Acid hydrolysis of Blanche Fleur, however, removed both, the readily detectable nitrile absorbance as well as the poultry feed-intake inhibition. This observation could potentially form the basis for a simple post-harvest detoxification process for V. sativa and other feed stuffs containing acid labile antinutritive factors.
Unfortunately, cases of poisoning by Vicia species continue to be reported. These can be grouped into those caused by V. sativa and its related species (cyanogenic glycoside Vicianine: HCN poisoning; and anti-nutritional effects of -cyanoalanine) and those caused by canavanine containing species (V. villosa, V. benghalensis, V. ervilia etc.). Farmers need to be made aware of the well documented biochemical distinctions between Vicia cultivars to prevent the accidental intoxication of their livestock with seeds containing high concentrations of canavanine or vicianine.
Finally, an overview of the voluminous and widely dispersed vetch literature, coupled with the observations in this thesis, suggest that the utility and value of each of the three Vicia model species examined in this thesis can be markedly enhanced by the following strategies:
1. Provision of sufficient alternative feed sources to allow feed intake to be regulated by palatability, thus minimising toxin ingestion.
2. Adaptation to Vicia toxins a) through selection of a digestive flora capable of detoxification (in the case of ruminants) and b) through selection or modification of animal genotypes with improved biochemical tolerance or even resistance to toxicity.
3. Detoxification prior to ingestion (Post-harvest detoxification)
4. Plant selection or genetic modification of specific toxin biosynthetic pathways to provide cultivars with optimum toxin concentration and distribution in strategic tissues (minimisation of toxins in the end product).
The inevitable conclusion from this thesis is that by incrementing our current fundamental knowledge of the biological chemistry of their naturally occurring anti-predator metabolites, we will promote the intelligent usage of Vicia species as highly nutritious grains for a sustainable agriculture.
This publication was originally submitted and accepted in July 1994 as a PhD thesis at the Waite Agricultural Research Institute, University of Adelaide, South Australia.
I would like to thank the many people who have contributed their time, thought and resources to the successful completion of this study. The many discussions with friends and colleagues, and the written correspondence with overseas researchers have helped to formulate and test many ideas.
Scientific collaboration with the late Dr. R. L. Davies, Dr. Phil Glatz, Lynne Giles and Dr. Nigel Maxted has been one of the key features of the study. Individual contributions are acknowledged in the relevant sections of this thesis. I would also like to thank the staff at the South Australian Department of Agriculture's Northfield Piggery and Parafield Poultry Research Centre, particularly Janine Baker and Andrew Cecil, for carrying out the animal experiments.
This study would not have been possible without the continuous help of Dr. Max E. Tate, whose initiative, stimulating ideas, encouragement, patience, experience, wisdom, guidance and friendship have made it a truly rewarding and unique experience.
The unique combination of skills and resources of the Waite Agricultural Research Institute, its staff and students have also contributed significantly to the outcome of this work. I am particularly indebted to the library staff for their help with the obtention of literature, to the services of the supply unit and to the administrative and technical support afforded by the former Department of Agricultural Biochemistry and the Department of Plant Science.
The financial support for this study through a postgraduate scholarship from the Australian Grain Research Development Corporation (GRDC) is gratefully acknowledged.
In addition, I would like to thank my parents for first introducing me to vetches; and their understanding and financial support for my oversees travels, which were also funded by contributions from the Alf Hannaford Bequest Fund and the Department of Plant Science. The generous help of my oversees hosts with their time, research collections, contacts and hospitality has also been invaluable.
Finally I would like to thank Dr. Clive M. Francis for making valuable suggestions to successive drafts of chapters 1 and 8 and the Centre for Legumes in Mediterranean Agriculture (CLIMA) for support during the final stages of writing.
Enneking, D. (1994) The toxicity of Vicia species and their utilisation as grain legumes. Doctoral Dissertation. University of Adelaide, South Australia.[scan of original document at Australian digital theses [ADT] portal]
Also published as Enneking, D. (1995)The toxicity of Vicia species and their utilisation as grain legumes. [PDF] Centre for Legumes in Mediterranean Agriculture (CLIMA) Occasional Publication No. 6, University of Western Australia, Nedlands W.A. [with chapter 4 missing]