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III. Estimates for Major Crops

III. Estimates for Major Crops

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Table I

Estimates of Nitrogen Firation by Forage Crops

Contml species



Duration of

experiment (years)



Location



~



16

II

6O



Geneva. NY

Lexington, KY

R m m o u n t , MN

Lexington. KY

Northern Ireland

Beltsville, MD



Collison cr d.,1933

Karralicr cr al.. 1954

Heichel cr d.,I 9 8 1

Karraker cr ol.. 1950

Halliday and Pate, 1976

Wagner. 1954

Karraker er 01.. 1950

S p g u e . 1936

chapman cr al.. I949

Sprague. 1936

Phillip and Bennca. 1978

Joms er al.. 1977

Rizk. 1%2



165- 189



Lysimeter

Lysimeter-differeme

Isotope dilution-"A"

Lysimeter-difference

C& reduction

Difference



154

I 7b

140

9b

21-183

207

62-235



Lysimter-difference

Difference

Lysrmeter

Difference

"A" value

Lysimete-difference

Difference



Winter wheat

Soh chess

Soh chess

chicory



3

2



Lexington, KY

New Brunswick. NJ

Riverside, CA

New Brunswick, NJ

Hopland, CA

Davis, CA

Giza,E g y p



21'



Difference



Winter wheat



5



New Bmnswick. NJ



Sprague, 1936



641



Difference



Winter wheat



5



New Brunswick. NJ



Sprague. 1936



Difference

Lysimeter

Lysimeter-differencc



Winter wheat



5

10



Kentucky bluegrass



II



New Brunswick, NJ

Riverside, CA

Lexington. KY



Sprague. 1936

chapman e r a / . , 1949

K&cr

ct d..1950



Alfalfa

(Medicago sariva)



229-290

212

I48



White clover

(Trifoliurn repms)

Ladin0 clover

(Trifoliurnrepens var. Ladino)

Red clover

(Medicago prmense)

Sweet clover

(Mclibrn a h )

Subclover

(Trifoliurn subrerraneurn)

Egyptian clover

(Trifolium alexandrinurn)

Alsike clover

(Trifolium hybridurn)

Crimson clover

(Trifoliurn indica)

Vetch

(Vicia vilbsa)

K o m kspedeza

(kspedew sripulacca)



I28

258



aDuration given in months.

*Winter crop rotation.



-



I lob



I84

193



Kentucky bluegrms

Reed canarygrass

Kentucky bluegrass



II



-



1



Orchard grass-call fescue



I



Kentucky bluegrass

Winter wheat



-



-



II

5



10

5

7'



HOW MUCH NITROGEN DO LEGUMES FIX?



29



tion in subclover (Trifolium subterraneum L.) at Davis, California. Over a

3-year period, subclover fixed 261, 398, and 207 kg N/ha, as estimated by

difference. The soft chess control (Bromus mollis L.) accumulated 37, 32, and

72 kg N/ha.

Sprague (1936) evaluated a series of legumes for their usefulness as winter

green manure crops in New Jersey. Over a 5-year period, winter wheat (Triticum

aestivum L.), hairy vetch (Vicia villosa), crimson clover (Trifolium incarnatum), red clover, alsike clover (Trifolium hybridum), and sweet clover were

planted in August following a corn crop. In April of the following year samples

of the tops and roots (to a depth of 28 cm) were harvested in N analysis. The

remainder of the crop was incorporated into the soil and the corn summer crop

was planted. Over the 5-year period, the average fixation by difference was 17,

9, 21, 64, and 110 kg N/ha for red clover, sweet clover, alsike clover, crimson

clover, and vetch. The relatively low rates of fixation are most likely due to

the winter cropping system used in this study. Hairy vetch was found to be

most suited to a winter green manure rotation.

Sears et al. (1965) reported an extremely high rate of 406-681 kg N/ha for

white clover in New Zealand (difference method-mixed grass control). These

figures were obtained, however, in an artificially depleted soil system. The top

15 cm of soil was removed, and the remaining subsoil was mixed with additional

subsoil and replaced. Thus the experimental system had an artificially lowered

soil N level. Additionally, these rates may exceed estimates from other locations

because the growing season was a full 12 months.

A white clover perennial ryegrass lye i n Northern Ireland fixed N for 8 months

(Halliday and Pate, 1976), but there was essentially no acetylene-reducing activity during November-February when the soil temperature averaged 4-5°C. Integration of the seasonal acetylene reduction profile indicated a fixation of 268 kg

N/ha.

Wagner ( 1 954) examined N fixation in ladino clover by the difference method

at Beltsville, Maryland. Over a 2-year period, the clover averaged 165-189 kg

N/ha.

A study by Rizk (1962) in Egypt estimated the fixation of two varieties of

Egyptian clover (Trifolium alexandrinum) utilizing the difference method with

chicory (Chicorium intybus) as a control. A considerable difference between the

cultivars was found, with the average nitrogen fixation ranging from 62-235 kg

N/ha.

Phillips and Bennett (1978) utilized the “AN value” technique and compared

it to acetylene reduction activity in rangeland plots of subclover and soft chess in

California. The influence of planting density and percentage clover in the plots

was also studied. The amount of N fixed (kilograms per hectare) was found to be

dependent on both stand density and composition. Low-density stands with 50%

clover fixed 21.2 kg N/ha and derived 84.5% of the clover N from fixation. A



30



THOMAS A. LARUE AND THOMAS G . PATTERSON



low-density stand of 100% clover fixed 58.1 kg N/ha but derived only 50.1% of

the clover N from fixation. High-density stands fixed 103 and 183 kg N/ha (94.5

and 88.0% clover N from N2) in 50 and 100% clover stands, respectively.

Estimates for alfalfa in a northern environment came from Heichel et al.

(1981) in Rosemount, Minnesota. They used isotope dilution and A N value to

estimate N fixation in two populations of alfalfa selected for high nitrogenase

activity. Reed canary grass (Phalaris arundinacea) was used as a control. Average N fixation in the establishment year was 148 kg N/ha, with an average of

43% of the nitrogen derived from fixation. Both the amounts of N fixed and

percentage of N derived from fixation varied over the season. Nitrogen fixation

was 8-20 kg N/ha at the first and fourth harvests (25-30% of plant N from N2).

During the second and third harvest period the legume fixed 47-87 kg N/ha (60%

of plant N from N2).

Estimates for forage legumes vary widely between studies. White clover, for

example, was reported to fix 128 kg N/ha in Kentucky and 408-681 kg N/ha in

New Zealand. Differences in climate, management practices, and growing season cause considerable variation in the N fixation rates of forage legumes. Direct

comparisons of the values in Table I therefore must be approached with caution.

B. SEEDLEGUMES

The soybean Glycine max is the most important cash crop among legumes in

North America, and its N fixation has received more attention than other crops.

Most studies do not lend themselves to estimates of amounts of fixation, though

several yield data on the percentage of N derived from fixation (Tables I1 and

111).

Rizk (1 966) used the difference method to calculate fixation by soybean in a

calcareous sand at Kutch, Egypt. Sesame (Sesamum indicum) was the nonfixing

control and soil N was measured before sowing and after harvesting. Rizk reported a fixation of 16.7 kg N/ha and a seed yield of 13.7 kg N/ha. These low

figures support his statement that he had not found the most suitable tillage

practice for this crop.

Weber (1966) compared the above-ground N content of a nodulating and a

near-isogenic nonnodulating soybean cv. Lee at Ames, Iowa, for 6 years. In 2

years when moisture was limiting, the difference was 14.7 kg N/ha, representing

about 13% of the plant N. In 4 years with good growth conditions, the mean

difference was 72.3 kg N/ha in seed or 84 kg N/ha in total dry matter. In both

cases this represented 40% of the total N in the nodulated plant. When the soil

was amended with 45,000 kg/ha of corn cobs to immobilize N, the average

difference in 3 years with good growth conditions was 160 kg N/ha in dry matter,

or 74% of the total N . This higher figure may illustrate a potential for fixation by



31



HOW MUCH NITROGEN DO LEGUMES FIX?

Table I1

Estimates of Nitrogen Fixation by Soybean



Location



Estimate

(kg N/ha)

39.7

14.7-84



Egypt

Iowa



Delaware



Method

Difference

Difference



GH, reduction



33-42

80- 120

103

56- I61



“ A ” value

Difference



Minnesota



263

I05

76-152



Difference

GH, reduction

“ A ” value



Nebraska



43-146



“A” value



Southern Ontario



78-161



C,H, reduction



Illinois

Arkansas

Washington



Remarks

Sesame

Nonnodulating

isoline, soil

low in N

Fertile soil



Nonnodulating

isoline

Uninoculated

Soil low in N

Nonnodulating

isoline

Nonnodulating

isoline

lnoculant trial



References

Rizk ( 1 966)

Weber (1966)



Hardy et a / . (1973)

Johnson et al. (1975)

Bhangoo and Albritton (1976)

Bezdicek et a / . (1978)

Ham and Caldwell (1978)

Deibert et al. (1979)

Muldoon et al. (1980)



soybean, but the extraordinary soil amendment is not representative of normal

practice.

Soybeans were grown in soils high in available N near Wilmington, Delaware,

and assayed by the acetylene reduction technique. In 3 years with a low planting

density, they fixed an average of 38 kg N/ha. In other trials with higher

planting densities, rates of 80- 120 kg N/ha were calculated. These approximated

to 25-30% of the total plant N (Hardy et a l . , 1973).

Table 111

Estimates of Nitrogen Fixation by Pulses



Pulse

Phaseolus vulgaris“

Pisum sativum

Vicia faba

Lupine

Chick-pea

Lentil

Arachis hypogea



“25-120 mg/plant.

bCalculated.



Estimate

(kg N/ha)

1Ob



17-69

121-171

121-157

67-141

62-103

79

87-222



Method



Reference



GH, reduction

GH, reduction

Difference (barley)

Difference (barley)

Difference (barley)

Difference (barley)

Difference (sesame)

Difference

(uninoculated check)



Westerman and Kolar (1978)

Mahler et al. (1979)

b z k (1 966)

Rizk (1966)

Rizk ( I 966)

Rizk ( I 966)

Rizk ( 1 966)

Ratner et al. (1979)



32



THOMAS A. LARUE AND THOMAS G . PATTERSON



Bhangoo and Albritton ( 1 976) compared nodulating and nonnodulating

lines of cv. Lee for 3 years at Pine Bluff, Arkansas. The N differences in seed

and dry matter were 130, 161, and 56 kg N/ha, representing 51, 64,and 22% of

total plant N. In the first 2 years the trials were at the same plots, whereas in the

third year the soybeans were planted on an area that had previously grown corn

and had been heavily fertilized with NPK. This latter figure is probably more

representative of the way soybean is generally grown.

A comparison of inoculated and uninoculated soybeans cv. Merit was made in

an irrigated low-N soil at Prosser, Washington (Bezdicek et al., 1978). The total

plant N was 368 and 105 kg/ha; the difference of 263 kg N/ha representing 71%

of the inoculated plant. An estimate based on acetylene reduction was 105 kg

N/ha. The threefold difference in seed yield and plant top N suggests that the

roots might not be comparable in the two treatments; perhaps inoculation provided sufficient N to support additional root growth to obtain soil N. In that case,

the difference method would overestimate fixation.

Ham and Caldwell (1978) tested cv. Clay at Rosemount, Minnesota, with

plots amended with I5N and with different P levels. Fixation calculated by the

“ A value” method was 76-152 kg N/ha. The authors reported that these results

agreed with measurements made by Kjeldahl N and by weekly acetylene reduction experiments made with the same variety on an adjacent plot.

In Nebraska, soybeans cv. Ford were grown with sprinkle irrigation (Deibert

er al., 1979), with rates of added N of 0-134 kg/ha. At the & (beginning seed)

stage, the total plant N was 70 and 178 kg/ha in nonnodulating and unfertilized

nodulating lines, respectively, and at the highest levels of fertilizer were 170 and

180 kg N/ha. A , value calculations indicated that fixation had contributed 60 and

33%, respectively, under the two regimes. At harvest, the difference in seed N

was 51 and 61 kg N/ha, and the percentage of N in seed from fixation was

calculated at 66% in unfertilized and 31% in fertilized plants.

Muldoon et al. (1980) compared a seed-applied inoculant and two soil-applied

granular inoculants at three sites in southern Ontario, Canada. The fields had not

been planted with soybean previously. Acetylene reduction assays indicated a

range of 12-17 kg N/ha in uninoculated plots. Fixation with the largest amount of

seed-applied inoculant was 78 kg N/ha. At the heaviest applications of two

granular soil inoculants, the fixation rates were calculated at 128 and 161 kg

N/ha. Differences in total plant N between inoculated and uninoculated plots

were usually lower than the N (GH,)calculated. Interestingly, the added yield

barely paid for the cost of granular inoculants if they were used at recommended

levels.

Four varieties of soybeans were grown in the field at Diome, France

(Amarger et al., 19791, and fixation was estimated from variations in natural

abundance. Yield figures were not presented, but fixation apparently contributed

13-37% of the plant N.

The effect of soil fertility and added fertilizer on the degree of symbiotic



HOW MUCH NITROGEN DO LEGUMES FIX?



33



fixation was estimated by isotope dilution at Urbana, Illinois (Johnson et al.,

1975). Soybeans in unfertilized fields fixed 48% of their N; this decreased to

10% as fertilizer rates increased to 224 kg N/ha. The authors concluded that the

upper figure was a good estimate for their region. Calculations indicated that

soybean is a good scavenger for soil N and that soybean removes larger quantities

of N from soil than corn does.

The natural abundance of I5N was measured in normal and nonnodulating

isolines of soybean cv. Harosoy at Urbana, Illinois. The percentage of N contributed by fixation was calculated by the N difference method and calculations from

isotopic concentrations (Kohl et al., 1980). In 2 years the N from fixation was 14

and 37% (by difference) or 33 and 43% (by W”). Depleting soil N by adding

corn cobs increased the fixation to 5 3 or 56% estimated by the respective

methods.

The studies listed here are from every soybean-growing area of North

America. Yields, when reported, were over 2000 kg/ha. Except when soil N was

low, the contribution of fixation rarely exceeded 50%. The average American

soybean yield (1975) was 1471 kg/ha. Assuming that the harvested seed represents about two-thirds of plant N, the whole plant N approximates 150 kg/ha on

farms. Since it is unlikely that fixation on farms is more than 50%, the upper

estimate for average fixation by soybeans in American agriculture is 75 kg N/ha.



I. Viciu faha L .

Faba beans use soil or fertilizer N in preference to symbiosis. Pot experiments

(Richards and Soper, 1978) show that they are as adept as barley in extracting

available N. In pots low in N, 87% of the plant N was derived from fixation ( A N

value method). Fertilizer addition decreased fixation without increasing total

shoot N.

In the field, faba bean yields are not responsive to added fertilizer. From this it

was assumed that symbiotic fixation was adequate and that “the nitrogen in the

grain is an approximate estimate of the atmospheric nitrogen “fixed” (McEwen,

1970). There was no experimental support for this view. The results of Sprent

and Bradford (1977) indicate that during pod fill fixation estimated by acetylene

reduction accounts for about one-third of the plant’s N gain.

Estimates in soils at Giya and Sids, Egypt, were based on crop and soil accumulation of N, compared to barley, and were in the range 49-171 kg N/ha (Rizk,

1966).



2 . Arachis hypogaea L .

Compared to sesame, peanuts at Kutah, Egypt, accumulated 79 kg N/ha in crop

and soil (Rizk, 1966).

In 3 years at Lakhish, Israel, the shoot N difference between uninoculated and



34



THOMAS A. LARUE AND THOMAS G . PATTERSON



inoculated peanuts was 222, 93, and 87 kg N/ha. These corresponded to 58,40,

and 30% of total N in the inoculated plants (Ratner et a l . , 1979). The highest

estimate of fixation was associated with a hay yield of 8667 kg/ha and a pod yield

of 7042 kg/ha containing 5056 kg/ha kernel. The soil was not low in nitrogen and

the crops were frequently imgated. The extraordinary yields suggest that the

estimates for total fixation should not be applied to typical peanut crops, which

have an average yield of 980 kg/ha (FAO, 1976).

3 . Pisum sativum L .



Mahler e f al. (1979) measured CpH, reduction in pea plots on the ridge top,

south slope, and bottomland of a catina near Pullman, Washington. The three

sites were within a few hundred meters of each other. The total plant N at the

three sites was 75, 99, and 210 kg/ha. The calculated fixed N was 17 (23%), 22

(23%), and 69 (33%) kg/ha. The lower yields on the ridge and slope were

associated with water stress. The differences in fixation observed within a small

region demonstrate the futility of extrapolating amounts fixed in agriculture from

single investigations.

4 . Phaseolus vulgaris L .



Acetylene reduction rates were estimated for 18 dry bean cultivars at Kimberly, Idaho (Westerman and Kolar, 1978). The calculated N fixation was in the

range 25-120 mg N/plant. Fixation on an area basis was not reported, but the

planting density was about 100,000 plants/ha. This suggests a fixation of about

10 kg N/ha, a small part of the total uptake of 150-400 kg N/ha.

Unfortunately there are few estimates of fixation by pulses important to farmers in developing nations. The accumulation of plant and top soil N in low-N

Egyptian soils was estimated by Rizk (1966). The rates of fixation by lupine

(121-157 kg N/ha), chick-pea (67-141 kg N/ha), and lentil (62-103 kg N/ha)

are not necessarily representative of the rates on farms. Cowpeas grown in a

greenhouse can fix 88% of their N (Huxley, 1980). Cowpeas are generally grown

as intercrops with maize or sorghum. Since the average yield of cowpeas is only

200 kg/ha (FAO, 1976), the amount of N fixed per hectare must be small.



IV. SUMMARY

A. EVALUATION

OF STUDIES



There is not a single legume crop for which we have valid estimates of the N

fixed in agriculture. There are good estimates for soybean grown in representative



HOW MUCH NITROGEN DO LEGUMES FIX?



35



locations in experimental plots. However, extrapolation from this data to fixation

in agriculture is speculative. For other pulses the few documented reports do not

permit estimation of fixation on farms.

The data on forage legumes are sparse and mostly derived from studies of pure

stands. Estimates from more locations are required. In practice the forages are

often planted with a grass, or over time become admixed by grasses. There is an

almost complete lack of data on fixation by mixed stands, or on the amounts of

fixation when forages are harvested or browsed.

It is regrettable that fixation by legumes, which are important to the developing

world, is not better documented. Dry beans are the most important legume crop

for human consumption in Latin America. Cowpeas are a staple in much of

Africa and Asia, and chick-pea is important in semiarid regions. For none of

these are data available.

There is no good evidence that any legume crop satisfies all its N requirements

by fixation. Soybean fixation has been estimated in several areas of the United

States and from consideration of all the data we must conclude that this crop

depletes soil N. There are no substantiated reports that 100% N of any plant

derives from symbiosis. The highest estimates (-80%) are typical of lowfertility soil or soils artificially made N-poor by admixture or carbon amendment.

B. REQUIREMENTS

FOR FUTURERESEARCH



Appropriate techniques for examining N fixation in perennial forage legumes

must be developed. The interpretation and accuracy of long-term isotope studies

needs to be evaluated. Since forage legumes are often grown in association with

perennial grasses, techniques for estimating N fixation and N transfer between

species need to be developed.

A simpler technique, such as the difference method using a nonnodulating

control, would find wide application if equivalence to the isotope procedures can

be confirmed. The identification and development of more nonfixing forage

genotypes should be a priority. Viands et al. (1979) have identified an ineffective nodulation character in alfalfa. Nonfixing strains in other species would be

valuable.

With the rising cost of N fertilizer, the potential of using legumes to increase

soil N becomes increasingly attractive. Green manure systems were once much

used to increase soil N (Sprague, 1936). A reexamination of the potential of

legumes as a soil N source is called for. Quantitative data on the contribution of

fixed N to the soil and to succeeding crops is needed for an adequate economic

analysis of green manuring.

Adequate methods of estimating fixation in pulses exist, but they are not yet so

simple and inexpensive as to be commonly used. The acetylene reduction assay

as now used requires too many samples over the growing season to be convenient



36



THOMAS A . LARUE A N D THOMAS G . PATTERSON



for analyzing many cultivar, strain, location, fertilizer, or environmental combinations. Nondestructive in situ measurements may be made with inexpensive

apparatus (Mahon and Salminen, 1980), but the calibration of this assay with N

fixed has not been accomplished.

In developed countries with access to the necessary apparatus, isotopic techniques are likely to become more common. The 615N method of natural enrichment should be tested as a method of estimating fixation in agriculture by sampling seeds and comparing them with cereal grain harvested in the same region.

This might serve as a way of estimating, albeit approximately, fixation over large

areas.

In developing countries there is need for inexpensive methods not requiring

expensive imported apparatus. The Kjeldahl method for N accumulation in plant

and soil would be useful if a way were found for estimating N mobilized from

lower strata. This can be accomplished most easily if in each geographic region

nonlegumes are found that utilize soil N in a manner similar to that of the major

legume crops. There is then an urgent requirement to test nonlegumes that might

serve as suitable controls for the difference method. Indirect methods based on N

compounds in legume shoots might be used if they could be calibrated with

fixation.

Plant physiologists should determine whether symbiotic fixation in the field is

more demanding of photosynthate than use of soil N. They should determine why

legumes prefer to use soil N, and why even low levels of available N will

decrease nodulation and fixation in the field. If this knowledge were available, it

might be possible to breed legumes, especially forages, that would supply more

of their N needs by fixation and leave soil N for grasses or cereals.

REFERENCES

We have omitted many articles and reviews stating estimates of symbiotic fixation without citing

the source of information. We have also left out estimates, often anonymous, in commercial

brochures and Institute or Station annual reports in which the experiment leading to the estimate is not

documented. We noted only a few of the many reports that assume, without evidence, that total plant

N, shoot N , yield, or some multiple of nodule weight, etc. is the measure of fixation.

Amarger, N., Mariotti, A . , Mariot’ti, F . , Durr, J. C., Bourguignon, C., and Lagacherie B. 1979.

Plant Soil 52, 269-280.

Bardin, R., Domenach, A. M., and Chalamet, A. 1977. Appl. Rev. Ecol. Biol. Sol. 14, 395-402.

Bezdicek, D. F . , Evans, D. W., Abede, B., and Witters, R. E. 1978. Agron. J . 70, 865-868.

Bhangoo, M. S . , and Albritton, D. J. 1976. Agron. J . 68, 642-645.

Bremner, J . M. 1965. In “Methods of Soil Analysis” (C. A . Black, ed.), Part 2, pp, 1149-1 179

and 1256-1286. Amer. SOC.Agron. Madison, Wisconsin.

Bums, R. C., and Hardy, R. W. F. 1975. “Nitrogen Fixation in Bacteria and Higher Plants.”

Springer-Verlag. New York.

Bums, R. H. 1972. I n “Methods in Enzymology” (A. San Pietro, ed.), Vol. 24, pp. 415-431.

Academic Press, New York.



HOW MUCH NITROGEN DO LEGUMES FIX?



31



Bums, R. H. 1978. In “Environmental Role of Nitrogen-fixing Blue-green Algae and Symbiotic

Bacteria” (U. Granhall, ed.). NFR Editorial Service. Stockholm.

Bums, R. H., and Wilson, P. W. 1957. In “Methods in Enzymology” (S. P. Colowick and N. 0.

Kaplan, eds.), Vol. IV, pp. 355-366. Academic Press, New York.

Chapman, H . D . , Liebig, G . F . , and Raynes, D. S. 1949. Hilgardia 19, 57-128.

Collison, R. C.. Beattie, H. G., and Harlan, J. D. 1933. N.Y. Agric. Exp. Sta. Tech. Bull. No. 212.

Cowling, D. W . 1961. J. Br. Grassl. Soc. 16, 281-290.

Craswell, E. T . , and Martin, A . E. 1975a. Aust. J. SoilRes. 13, 43-52.

Craswell, E. T., and Martin, A . E. 1975b. Aust. J. SoilRes. 13, 53-61.

Deibert, E. J. Bijeriego, M . , and Olson, R. A. 1979. Agron. J . 71, 717-723.

de Souza, D. I. A. 1969. East Afr. Agric. For. J . 34, 299-305.

Domenach, A. M . , Chalamet, A., and Pachiaudi, C. 1979. C.R. Acad. Sci. (Paris) D289,291-293.

Erdman, L. W. 1949. USDA Farmers Bull. No. 2000, pp. 1-20.

F A 0 1976. “1975 Production Yearbook,” Vol. 29. Food and Agricultural Organization of the

United Nations, Rome.

Fried, M., and Dean, L. A. 1952. Soil Sci. 73, 263-271.

Fried, M., and Middelboe, V. 1977. Plant Soil 47, 713-715.

Halliday, J . , and Pate, J. S. 1976. J. Br. Grassl. SOC.31, 29-35.

Ham, G. E., and Caldwell, A. C. 1978. Agron. J. 70, 779-783.

Hardy, R. W. F., and Havelka, U. D. 1975. In “Symbiotic Nitrogen Fixation in Plants” (P.

Nutman, ed.), Int. Biol. Prog. Ser. Vol. 7, pp. 421-439. Cambridge University Press, London.

Hardy, R. W. F., Bums, R. C., and Holsten, R . D. 1973. Soil Biol. Biochem. 5, 47-81.

Hauck, R. D., and Bremner, J. M. 1976. In “Advances in Agronomy” (N. C. Brady, ed.), Vol. 28,

pp. 219-266. Academic Press, New York.

Heichei, G. H . , Barnes, D. K.,and Vance, C. P . 1981. Crop Sci. 21, 330-335.

Henzell, E. F. 1962. Aust. J. Exp. Agric. Anim. Hush. 2, 133-140.

Hudd, G . A., Lloyd-Jones, C. P., and Hill-Cottingham, D. C. 1980. Physiol. Plant. 48, 1 I 1-1 15.

Huxley, P. A . 1980. Trop. Agric. 57, 193-202.

Jones. M. B., Delwiche, C. C . , and Williams, W . A. 1977. Agron. J . 69, 1019-1023.

Johnson, J. W . , Welch, L. F., and Kurtz, L. T. 1975. J. Environ. Q u a / . 4, 303-306.

Kamprath, E. J . , Chandler, W. V., and Krantz, B . A. 1958. N.C. Agric. Exp. Sta. Tech. Bull. No.

129.

Karamanos, R. E., and Rennie, D. A. 1980. Can. J. Soil Sci. 60, 337-344, 365-372.

Karraker, P. E . , Bartner, C. E., and Fergus, E. N . 1950. Kentucky Agric. Exp. Sta. Bull. No. 557.

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