The contribution of any N2-fixing plant to the sustainability of agricultural systems depends on how much of the fixed N is harvested and removed from the system. For grain legumes the amount of N contributed is the amount of N2fixed less the amount of N harvested in the seed (Myers and Wood, 1987). This can be simply restated as ‘the %N from N2-fixation must be greater than, or equal to, the percentage of total legume N removed in the grain’, which is a useful ‘rule of thumb’
to indicate whether there are net benefits to the system of growing a legume (Giller et al., 1994). Such calculations ignore inputs below ground (see below) but serve to indicate that many grain legumes, particularly those that are most efficient at packaging their N into the grain (such as soybean), may actually remove more soil N in the grain than they contribute to the soil through N2-fixation (Peoples and Craswell, 1992; Giller and Cadisch, 1995). If all of the above-ground plant material is removed, including the crop residues, there are few cases where a net contribution from N2-fixation will be made.
This approach does not have to be confined to examining effects on N alone. A lot of research effort has been directed to calculation of budgets for major nutrients in farming systems in the tropics in recent years (Smaling, 1998). As the soil contains so much N in organic form, often 5000–10,000 kg N ha-1or more, small changes in the N status of the soil are difficult to measure or take into account in N balances.
Other problems with this approach derive from the complexities of measuring losses of N from systems through leaching, gaseous transfers and eroding soil. Long-term field experiments comparing cropping sequences with and without the N2-fixing plant are the most powerful way of employing N balances, but there are few such experiments in the tropics (Leigh and Johnston, 1994).
Inputs from N
2-fixation in Simultaneous Systems
The advantages of growing N2-fixing plants in mixtures result from many factors in addition to possible benefits from N2-fixation, including more efficient capture and use of resources for growth, such as light and water (Reddy and Willey, 1981;
Marshall and Willey, 1983), and pest control due to avoiding a monoculture (Altieri et al., 1978). The advantage of intercrops over sole crops is commonly expressed in terms of the land equivalent ratio (LER), which is simply an expression of the land required for production of the same yield in the sole crops compared with the inter- crop (Willey, 1979). If more land is required when plants are grown as sole crops, then the LER is > 1 and the intercrop is advantageous. The LER is also sometimes calculated and expressed as the relative yield total (RYT), which is mathematically the same as the LER. An extension of the concept of the LER has been to take account of
the length of time during which the land is occupied by the crops (Hiebsch and McCollum, 1987), which is important when the growing season is sufficiently long for more than one crop to be grown. When using these approaches, care must be taken to grow the crops at their optimal densities in both sole stands or mixtures, otherwise the advantages of intercropping may be overestimated (Onget al., 1996).
Of course, the economic value of crops must also be considered when evaluating benefits from intercrops.
The interactions between crop species can be divided into: (i) competitive interactions, in which the crops compete for the same resource; and (ii) facilitative interactions, in which one crop alters the environment of the other in a positive way so as to benefit the growth of the other species (Vandermeer, 1990). Most of the benefits of growing crops in intercrops come from the way that they complement each other in their exploitation of the environment – for instance, by rooting to different depths and thus exploiting different parts of the soil, or by having leaf canopies at different heights, which might increase the total amount of light inter- cepted, leading to greater overall resource capture. In such examples the benefits of intercropping are due to weak competition for resources. As we shall see, there is considerable controversy as to where the benefits from N2-fixation fit within this framework; that is, whether the benefits are due to the N2-fixing plant ‘sparing’ soil N, or due to a direct contribution of fixed N for use by the other crop. Virtually all the research that has examined N transfer from N2-fixing plants in plant mixtures has been focused on mixtures of legumes and grasses or cereals.
N transfer in legume/cereal intercrops or mixed legume/grass swards Several researchers have claimed a significant role for direct nitrogen transfer of fixed N from the legume to the intercropped cereal (e.g. Agboola and Fayemi, 1972). Early experimental work such as that of Virtanenet al. (1937), using N balance studies, indicated large amounts of N transfer in pea/cereal mixtures. Later evidence for significant transfer of N from cowpea to maize was based on comparison of the15N enrichments of the sole and intercropped cereal crops following application of
15N-labelled fertilizer (Eagleshamet al., 1981). The intercropped maize had a larger N yield and a smaller15N-enrichment, showing that it had taken up more unlabelled N than the sole maize crop. It was concluded that this unlabelled N had been excreted by the cowpea, which was depleted in15N due to fixation of atmospheric
14N2. However, it is equally possible that it was due to a sparing of soil N, perhaps from deeper in the soil where cowpea roots were not active and where the applied
15N-enriched fertilizer did not penetrate. In agreement with the latter interpretation, other workers concluded that it was not possible to calculate N transfer in intercrops by isotope dilution, due to doubts over the matching of N uptake patterns between cereals and legumes which would invalidate the estimates (Papastylianou, 1988).
Despite this, the isotope dilution method continues to be used in such studies.
If benefits from N2-fixation can be explained in terms of sparing of soil N, then this is effectively an example of weak competition due to the legume having an
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alternative source of available N (Vandermeer, 1990). There are few studies in which direct facilitative transfer of N from the legume to the cereal has been unequivocally demonstrated, and none carried out in the field. Van Kesselet al. (1985) used a split-root system and fed half of the soybean roots with15N-enriched nitrogen. Maize was grown together with the roots not fed15N and so the15N-enrichment found in the maize roots and shoots must have come from the15N-labelled soybean N. The
15N-enrichment of the maize was more than doubled when the plants were inocu- lated with vesicular–arbuscular mycorrhiza, but again the amounts of N transferred were small.
A direct method of measuring N transfer was proposed by Ledgardet al. (1985a) in which15N-labelled N is applied to the legume leaves and N transfer is detected by analysing for15N in the associated grass or cereal. Transfer of N betweenPhaseolus beans and maize was easily demonstrated using this sensitive technique but less than 5% of the bean N was found in the maize plants after several weeks – even under conditions of severe N deficiency (Gilleret al., 1991). In the same study, experiments using15N isotopic dilution only demonstrated significant N transfer from beans to maize when the plants grew poorly due to a severe pest attack, a similar finding to Wilson and Wyss (1937), who only found N transfer when the plant growth was reduced by shading. These results are surprising in that it might be expected that more N would be available for underground transfer when the growth of the legume is more vigorous. A possible explanation is that the pest attack or shading caused pre- mature nodule senescence, so releasing significant amounts of N to the intercropped cereal. Thus there is little direct evidence that facilitated transfer of N from legumes is generally important in the N nutrition of cereals in intercrops (Chalk, 1996b).
Much more attention has focused on mixtures of grasses and legumes (Chapter 10). Most evidence for significant benefits of N transfer has been based on the N difference method – that is, on comparisons of the N economy of pure or mixed grass swards (e.g. Birch and Dougall, 1967) – or on an isotope dilution method in which a comparison of isotope enrichment of pure or mixed grass swards is made after the soil has been labelled with 15N-enriched fertilizer. Estimates of the amount of N transferred vary enormously, from no transfer being found in clover/ryegrass swards (Haystead and Lowe, 1977) to estimates of 20–50% (Ta and Faris, 1987a; Burity et al., 1989) or over 80% of the grass N being derived from the legume (Broadbent et al., 1982). All of these estimates were made using isotope dilution and are subject to the assumption that the uptake of soil and fertilizer N by the grass is not altered in the presence of the legume. There is evidence to suggest that rates of mineralization of organic N in soil may be greater in the presence of N2-fixing legumes (Ismaili and Weaver, 1986; Jensen and Sørenson, 1988; see above), which would mean that this assumption is not valid in such experiments. Perhaps more importantly, N uptake patterns may differ between the sole grass and the grass in the mixture, particularly where15N fertilizers have been sprayed on to the surface of a sward. Although these errors will be relatively small if rates of fixation are high (Boller and Nosberger, 1988), the isotope dilution method rarely seems to give accurate measurements of N transfer (Chalk and Smith, 1994).
Using the 15N foliar labelling method, Ledgard (1991) showed that under- ground transfer of N between white clover and ryegrass was greatest during dry, warm conditions. In the productive grazed pasture studied, the clover fixed 270 kg N ha-1 annually and there was an underground transfer of 70 kg N ha-1 compared with 60 kg N ha-1 transferred above ground via cow excreta. The repeated defoliation under grazing is likely to stimulate senescence and turnover of fine roots and nodules and to increase the availability of legume N for the grass. Indeed, significant transfer of N in mixtures of the forage legumeStylosanthes guianensisand the grassBrachiaria decumbenswas detected only when the legume was killed by cutting and removing the whole shoots (Tranninet al., 2000).
Mechanisms for underground ‘transfer’ of N
The degree to which N transfer is due to ‘excretion’ of N from legume roots is a mat- ter of some controversy. It has been known for a long time that exudates from legume roots contain N in the form of simple amino acids (Rovira, 1956) but such demon- strations are necessarily limited to carefully controlled laboratory experiments. Exper- iments in which movement of N from a legume to a grass was measured over periods of 1 week (Taet al., 1989) or longer (Ta and Faris, 1987b) were purported to provide evidence for a role of excretion in N transfer on the grounds that these were relatively short time periods. Whether this evidence can be taken to demonstrate excretion of N depends on the rate at which nodule and root tissues senesce and are lost to the soil.
The use of the term excretion is perhaps unfortunate as it implies an active loss of nitrogenous compounds, and it is hard to envisage any direct evolutionary benefit for the legume. Many authors have preferred to use the general term ‘rhizo- deposition’ to include exudation and passive losses, such as loss of structural tissues, because of the difficulty of separating the processes experimentally, and because of the relatively small contribution of exudation to total loss of carbon from the roots.
Jensen (1996) labelled pea and barley plants with15N by growing part of the root system in a separate chamber and feeding with a labelled N solution. Rhizodeposition was estimated to amount to 7% of the N in the pea plants, and roughly half of the below-ground N at plant maturity.
If one adopts the term rhizodeposition in this discussion, the controversy over ‘direct transfer’ evaporates, and the majority of the evidence does indicate that significant losses of N from legumes to the soil occur in the form of dead and senescent material. An exception is the evidence for the involvement of mycorrhizas in enhancing the transfer of N between legumes and grasses (Van Kesselet al., 1985;
Haysteadet al., 1988), which may possibly take place by hyphal interconnections between plant roots (Franciset al., 1986; Heap and Newman, 1986), although this again is controversial (Newman and Ritz, 1986). The amounts transferred by this mechanism are in any case unlikely to be of agronomic significance (Frey and Schüepp, 1993).
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