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VII. Nitrogen Transformations in Grassland Soils
THE MICROFLORA O F GRASSLAND
1964; Whitman and Stevens, 1952). The latter workers found 27 species
of legumes in western North Dakota grassland. Half of the total legume
productivity, which ranged from 25 to 90 kg/ha, was accounted for by
four species of legumes. Legume productivity usually accounted for less
than 10% of the total range productivity and at times, for no more than
I %. In quadrat counts, legumes averaged about 30 stalks/m2,whereas the
grasses showed from one thousand to several thousand stems/m2. Although of minor importance as structural components in grassland, the
legumes present therein are generally well nodulated, have deep, extensive root systems, and show an active period of growth during the
moist season. Although the amount of nitrogen fixed annually in the leguminous nodules may be quite low, nevertheless their cumulative role in
nitrogen accretion over a number of years can be substantial. Hopefully,
the recent advances in methodology will shortly make available more informative data on the amount of nitrogen fixed in leguminous symbioses
in various types of grassland.
Plants other than legumes may also serve as hosts for nodulating organisms (Bond, 1967; W. D. P. Stewart, 1966, 1967). Although the microbial endophytes involved in nonleguminous symbioses are not as yet
adequately defined, a wide variety of associations is postulated (Table
XVIII). For plants such as Alnus and Ceanothus, the nodulating bacteria
are actinomycetes rather than rhizobia. Eleagnus and Shepherdia are rootnodulating shrubs of this type and both are widely distributed throughout
many areas of grassland habitat. Recently, Farnsworth and Hammond
( 1 968) have reported that sagebrush (Arternisia lodviciunu) and prickly
pear cactus (Opuntiu frugilis) bear root nodules that appear capable of
fixing atmospheric nitrogen. If their observation is substantiated, it will
extend the range of nonleguminous symbioses and should encourage the
search for other associations. Species of Artemisia and Opuntia are widely distributed throughout the western Great Plains. Mayland et al. (1 966)
noted an increase of 15N in Artemisia during studies of fixation by algae
in Arizona desert but attributed the enrichment of isotopic nitrogen to
utilization of nitrogen which has been fixed and excreted by the algal
The leaf nodules and wet leaf surfaces of vegetation in humid tropical
regions provide suitable sites for the development of nitrogen-fixing
bacteria such as Azotobacter, Beijerinckia, Clostridium, Klebsiella, and
Xanthomonas (Ruinen, 196 1 , 1965; Silver el ul., 1963: Vasantharajan
and Bhatt, 1968). It is doubtful that phyllosphere floras contribute significantly to nitrogen accretion in semiarid grassland.
Mycorrhizal nitrogen fixation has been postulated from field evidence
FRANCIS E. CLARK A N D ELDOR A. PAUL
concerning the ability of Pinus species that bear mycorrhizae to grow
vigorously in nitrogen-poor soil (G. Stevenson, 1959). In his reviews on
Known or Postulated Nitrogen-Fixing Symbioses or Associations
Involving Nonleguminous Plants
Symbioses or associations involving
Alnus, Casuarina, Ceanothus,
Myrica, Shepherdia; possibly
Arremisia and Opuntia
Dryas, A rctosraphylos,
Fungus? (Saxton, 1930);
Numerous and diverse genera
of both graminous and nongraminous plants
N-fixing organisms in
Associations involving lower plants
Site of microbiont and
Root nodules are
Coralloid root hypertrophies
The lichen thallus,
which is a fungusalga symbiosis
'Nitrogen fixation is assumed on the basis of ecological observations, but definitive proof
*The microbionts involved (Azotobacrer, Beuerinckia, Closiridium, blue-green algae) are
known to fix nitrogen even if not in association with higher plants, but association with
higher plants is believed to augment their ecological role as fixers of nitrogen.
THE MICROFLORA O F GRASSLAND
nitrogen fixation by higher plants other than legumes, Bond (1967, 1968)
has cited evidence that podocarp nodules, containing a phycomycetous
nonseptate endophyte, fix nitrogen by means of a mycorrhizal association.
Mycorrhizae are known to occur widely among the grasses (Nicolson,
1959: Dorokhova, 1967), but thus far there is no good evidence that they
are capable of fixing atmospheric nitrogen.
Lawrence et al. ( 1 967) have considered the role of Dryas in vegetation
development on newly exposed mineral soil following glacier ice recession. Nitrogen turnover measurements in marine and brackish environments (W. D. P. Stewart, 1967) and studies of fixation by Hippophae in
dune sand (W. D. P. Stewart and Pearson, 1967) have shown fixation
ranging from a few to 100 kg of nitrogen per hectare to occur in these
nonleguminous communities. Nevertheless, at the present state of knowledge, leguminous symbioses must be considered as more important for
nitrogen accretion in grassland than are the various nonleguminous symbioses involving higher plants.
2 . Asymbiotic Nitrogen Fixation
Recognition of the paucity of legumes in many grassland areas has led
to a continued interest in the role of asymbiotic bacteria and other simple
plants in the nitrogen economy of grassland soils. Moore (1966) has summarized extensive data concerning asymbiotic nitrogen fixation in a wide
variety of soils. Many of the earlier experiments were based on Kjeldahl
measurements of long-term field plots. They tend to show a nitrogen imput averaging about 22 kg/ha annually. In this total is included the nitrogen accruing from rainfall, an imput which in itself can be considerable
(Eriksson, 1952; Junge, 1958; Mackenthun, 1965). Allison (1953, although not doubting that asymbiotic fixation does occur, expressed skepticism on the validity of many of the older measurements showing gains
of nitrogen ranging up to 100 kg/ha per year. It is now generally agreed
that the use of isotopic nitrogen or acetylene methodology is necessary
in order to obtain meaningful measurements of nitrogen fixation.
Delwiche and Wijler (1956) conducted 15Nz fixation experiments on
grass sod and associated cultivated soils and found no nitrogen fixation
to occur asymbiotically unless a source of energy, such as glucose, was
added. More recently, W. A. Rice et al. (1967), also using isotopic nitrogen, measured 19 pg of N per gram of soil fixed in 28 days in laboratory
samples of a prairie soil containing straw residues of the most recent crop.
The addition of higher concentrations of straw or waterlogging greatly
increased the rate of fixation (Table XIX). R. J. Myers et al. (1970)
measured nitrogen fixation in undisturbed soil cores 15 cm in diameter
Measurements of Asymbiotic Nitrogen Fixation Using I5N or C2H, Methodology
W. A. Rice et al. ( I 967)
R. J. Myers et al. ( 1 970)
Mayland et al. ( 1966)
Shtina et al. (1968)
Soil aliquots given laboratory incubation
(a) At field capacity, plus 1% straw
(b) At field capacity, plus 5% straw
(c) Waterlogged, plus 1% straw
(d) Waterlogged, plus 5% straw
15-cm diameter undisturbed soil cores
(a) Nostoc surface crust only
(b) 0-2.5 cm deep
(c) 2.5 cm deep
(d) Total 7.5 cm core, and using C Z H Z
15-cm diameter core of cultivated soil plus
2% wheat straw
(a) 0-2.5 cm deep
(b) 2.5-7.5 cm deep
(c) 7 5 cm deep
Algal crusts of Arizona desert
Algal crusts on chestnut soil, USSR
Algal crusts on rendzina soil, USSR
Mountain meadow (Colorado, U.S.A.) soil
block containing algae in moss habitat
Savanna (Nigeria) soil incubated moist and
with 35% oxygen
Sand dune (U.K.) marine environment
dominated by Nostoc, 0-1 cm depth
Jordan Fertility Plots (Pennsylvania, U.S.A.)
(a) No fertilizer added, 0-15 cm depth
(b) 27 kg/ha of N added, plus PK
(c) 81 kglha of N added, plus PK
Porter and Grable ( I 969)
Odu and Vine ( 197 I )
W. D. P. Stewart (1967)
Hardy et al. (1968)
(pglgram of soill28 days)
THE MICROFLORA OF GRASSLAND
and found (Table XIX) lower nitrogen gains than were found by W. A.
Rice et al. According to Myers and co-workers, the top 7.5 cm of cultivated soil amended with straw and incubated in a normal, controlled atmosphere fixed nitrogen equivalent to 0.6 kg/ha during 28 days of incubation. The same clay soil contained Nostoc crusts which fixed 239 pg of
N per gram of Nostoc crust. In the natural field soil, no fixation occurred
below 2.5 cm. The accumulated value of nitrogen fixation, as measured
by 15N, in the Nostoc crust and in the top 2.5 cm of soil, was 1.52 kg/ha.
Measurement of fixation in the same soil by the acetylene technique indicated 1.8 kg of N per hectare was fixed during equivalent time.
Data from other recent experiments utilizing I5N and C2H2
to measure fixation are also summarized in Table XIX. To present the
information in a comparable form, data from the various authors have
been recalculated on a micrograms per gram basis. Also further to facilitate comparison, data for incubation intervals longer or shorter than 28
days have been recalculated to 28 days.
The microflora involved in asymbiotic nitrogen fixation is diverse. At
least 15 genera of bacteria and many blue-green algae are now known to
fix nitrogen. The classical nitrogen-fixing organism Azotobacter and the
more recently isolated Beijerinckia occur sporadically and in low numbers
in grassland soils (Ross, 1960; Di Menna, 1966; W. D. P. Stewart, 1969)
and in soils generally. Exceptions are soils of the Nile Delta and sugarcane soils of Brazil in which high populations of Azotobacter and/or Beijerinckia occur. In semiarid grassland, neither genus is believed to be of
importance in nitrogen fixation.
Members of the genus Clostridium are widely distributed in grassland
soil (Di Menna, 1966; Campbell et al., 1967; Ross, 1958, 1960). They
can utilize the breakdown products of natural substrates, such as straw
(W. A. Rice et al., 1967), to fix large concentrations of nitrogen. The
clostridia are doubtless the most prolific nitrogen-fixers of the asymbiotic
bacteria. Members of the genera Pseudomonas, Achromobacter, Klebsiella, and Bacillus can readily be isolated on nitrogen-free agar (MeiMejohn, 1968; Paul and Newton, 1961; Moore, 1966; Anderson, 1955), but
they appear of doubtful effectiveness as nitrogen-fixers in field soil. The
significance of such organisms as Methanobacterium and Desulfovibrio
probably is not large. The photoautotrophic bacteria are widely distributed in aquatic environments but their functional occurrence in semiarid grasslands has not been demonstrated. Metcalfe and Brown (1957)
described two Nocardia species from grassland that were able to fix
atmospheric nitrogen. Fedorov and Ilina ( 1 960) also noted evidence of
nitrogen fixation by actinomycetes, but Jensen ( 1965) concluded that
FRANCIS E. CLARK A N D ELDOR A. PAUL
evidence for nitrogen fixation by nonsymbiotic actinomycetes is mostly
negative or unconvincing.
Various species of blue-green algae are known to fix atmospheric
nitrogen (Burris, 1956; Moore, 1966; Shields and Durrell, 1964; Shields
et al., 1957; Russell, 1950; Hernandez, 1956). Cameron, Mayland and
associates have calculated that algal surface crusts collected from Arizona desert rangelands could fix up to 10 kg/ha of nitrogen annually if the
soil surface was fully covered with such crusts (Cameron and Fuller,
1960; Fuller et al., 1961; Mayland and McIntosh, 1966; Mayland et al.,
1966). Since native rangeland is by no means fully covered by Nostoc or
other crusts, their calculated value must be scaled down considerably for
field conditions. Porter and Grable (1969) found algae contributed during
10 days approximately 4 kg of nitrogen per hectare in a wet mountain
meadow in which conditions were very favorable for algal growth. Liverworts and mosses may variously contribute to nitrogen fixation. Bond
and Scott (1955) found the liverwort Blasia pusilla capable of fixing
Moore ( I 966) and W. D. P. Stewart ( I 966) have discussed the contribution that the photosynthetic lower plants may make to nitrogen
fixation in various natural environments.
Heterotrophic nitrogen-fixers appear to play their major role by being
widely distributed and fixing small or very small quantities of nitrogen
over prolonged periods, particularly in microhabitats containing available substrates and restricted oxygen (W. D. P. Stewart, 1969; W. A.
Rice et al., 1967), possibly in the rhizosphere (Mishustin, 1967), and in
the case of the photosynthetic lower plants, singly or in mixed associations, in microhabitats of favorable light intensity and with high moisture,
at least intermittently.
Many workers have reported that there is an inhibition of nitrification
in grassland soil (Lawes, 1889; Miller, 1906; Lyon and Bizzell, 1918;
Richardson, 1938; Parberry, 1945; Theron, 195 1 : Theron and Haylett,
1953: Soulides and Clark, 1958; Woldendorp, 1962; Boughey et al.,
1964; E. L. Rice, 1964, 1965; Munro, 1966; Neal, 1969). In such soil,
the nitrate content is commonly observed to be negligible or absent while
the ammonium content, although small, is usually of measurable quantity.
This is in contrast to most cultivated soils, in which more of the mineral
nitrogen is to be found in the nitrate than in the ammonium form.
Various explanations have been offered for the relatively poor nitrification that occurs in grassland soil. T h e most commonly supported hypothesis is that there is direct suppression of the nitrifying bacteria by the
THE MICROFLORA O F GRASSLAND
living plant root. This was first suggested by Lyon and Bizzell(l9 18) and
Lyon et al. (1923) and was later endorsed by Theron (195 1 ) and Theron
and Haylett (1953). In recent years other workers have presented data
showing that exposure to either intact plant roots or to aqueous extracts
prepared therefrom influences the activity of the nitrifying bacteria
(Novogrudskii, 1963: Molina and Rovira, 1964; E. L. Rice, 1964, 1965;
Boughey et al., 1964; Munro, 1966; Neal, 1969).
Varying degrees of inhibition of nitrification by grass roots have been
reported. Munro (1966), working in Africa, found that all of the seven
grass species tested inhibited nitrification. In short-term experiments
involving exposure of nitrifiers to aqueous extracts of grass roots, oxidation of both ammonium and nitrite nitrogen was strongly to very strongly inhibited (Table XX). In contrast, Neal (1969) found that while the
native dominant grasses in western Canada failed to depress nitrification,
grasses and forbs that increase on or invade overgrazed land commonly
produced nitrification inhibitors.
Influence of Aqueous Extracts of Grass Roots on
the Activity of Nitrifying Bacteria"
Nitrite N produced
Nitrite N oxidized
Data of Munro ( 1 966).
Other workers have expressed doubt that inhibitions of nitrification
are caused by toxins of root origin and indeed some even doubt the occurrence of any such inhibition in grassland. Brar and Giddens (1968)
undertook to extract possible inhibitors from grassland soil but following
extraction, noted no improvement in the nitrifying capacity of the soil.
They concluded that the low nitrifying capacity in their soil was caused
by soil acidity and a low population of nitrifiers. Ross (1958) also believed
FRANCIS E. CLARK A N D ELDOR A. PAUL
that the low nitrifying potential of some grassland soils was due simply
to their acidity. Parberry (1945) and Michniewicz (195 1 ) believed there
might be insufficient aeration for good nitrification in grassland soils
covered by a layer of decaying plant residues. Harmsen and van Schreven
(1955) doubted the validity of any such explanation, since well-drained
grasslands generally have good aeration, often far superior to that of
O’Connor et al. (1962) and Robinson (1963) suggested that the low
production of nitrate in grassland was linked to a low population of nitrifying bacteria caused by the scarcity of ammonium ions in grassland and
the direct competition of grass roots for such ions. Chase et al. (1967)
found that grasses grown in Ontario, Canada, did not compete for ammonium to the detriment of the nitrifiers nor did the grass roots inhibit
nitrifiers by other means. Populations of nitrifiers in urea-treated grass
and fallow plots were fully comparable. It would appear that the mechanisms by which and the extent to which different grassland soils inhibit
nitrification are in need of further study. Presently the bulk of the evidence is that such inhibition does exist and, as E. L. Rice ( 1 965) and Neal
(1969) have pointed out, possibly the inhibitory effect may be of importance in conserving the low amount of available nitrogen present in grassland soils or in determining the success of individual species to invade
or to establish dominance in plant communities.
The three general pathways for gaseous losses of nitrogen from soil
are those of enzymatic denitrification, chemodenitrification, and volatilization of ammonia. Recent reviews concerning these pathways are
available (Broadbent and Clark, 1965 : Gardner, 1965).
1 . Enzymatic Denitrifcation
In order for enzymatic denitrification, a process in which microorganisms turn to a nitrate respiration in lieu of an oxygen respiration, to occur,
it is necessary that nitrate be present, that oxygen be absent or greatly
limited in its availability, and that sufficient available substrate or energyyielding material be present to permit microbial activity. Additionally of
course, such environmental factors as moisture, temperature, reaction,
etc. must be favorable for microbial activity. Grassland soils, particularly
those of semiarid rangelands, are characteristically low in nitrate, and
they are usually well aerated. Accordingly, enzymatic denitrification in
them can be expected to be negligible. However, should nitrate be present
and should there be either regions or microsites of poor aeration, the de-
THE MICROFLORA OF GRASSLAND
nitrification process should not be greatly limited because of any shortage of microbial substrate (Greenland, 1958, 1965). Grassland soils
usually contain considerable amounts of organic matter in the upper few
centimeters of the profile.
Chemodenitrification involves loss of gaseous nitrogen to the atmosphere due to nitrite instability (Clark, 1962). Inasmuch as the nitrite
dismutation requires the presence of nitrite and is promoted by microbial
metabolism (Clark and Beard, I96 I ) , chemodenitrification occurs primarily in soils in which the nitrification process is sufficiently retarded
to permit the accumulation of nitrite as an intermediate product in the
transformation of ammonium to nitrate and in which the organic matter
content is sufficiently high to support an active microflora. The inhibition
of nitrification that occurs in grassland soil, discussed above, is often
characterized by nitrite accumulation (Clark et al., 1960). In the work of
Soulides and Clark ( I 958), the gaseous nitrogen loss via chemodenitrification in some laboratory lots of grassland soils treated with urea nitrogen
was more than twice that measured for nearby intertilled soil.
Even though chemodenitrification losses of considerable magnitude
can be measured in the laboratory (Reuss and Smith, 1965: Soulides and
Clark, 1958; Wullstein and Gilmour, 1964), at present there appears to be
no justification for attempting to extrapolate such laboratory data to
finite values in the field. Most grassland soils do not receive ammoniacal
fertilizers and therefore such soils seldom if ever contain appreciable
nitrite. Only in grassland receiving ammonium nitrogen and in addition
characterized by a poor nitrifying capacity would any serious nitrogen
loss via chemodenitrification be expected. Even then, should warm temperature and drying conditions prevail, losses via ammonia volatilization
doubtless would be of much greater magnitude.
3. Volatilization of Ammonia
The loss of gaseous ammonia from soil is basically a physicochemical
process controlled by meteorological conditions and soil characteristics
(Gardner, 1965; Mortland, 1958). Microorganisms are involved to the
extent that they contribute to the supply of ammonium ions in the soil
by producing enzymes that hydrolyze urea or by decomposing soil organic matter. Microbial release of ammonium nitrogen from soil organic
matter occurs at a rate that is usually less than one or more of the following: the concurrent rate of nitrogen demand by growing plants; the
ammonium retention capacity of the soil: and/or the ammonium-oxidizing
FRANCIS E. CLARK A N D ELDOR A. PAUL
potential of the chemotrophic nitrifying bacteria in the soil. Because of
these demands, volatilization of ammonia microbially released from soil
organic matter can rarely be expected to occur.
Volatilization of ammonia is known to occur from grassland soils given
surface applications of urea or aqua-ammonia (Allison, 1955, 1966; Volk,
1959, 1961). There is usually a high urease content in grassland litter:
consequently, ammonia volatilization is usually higher from grassland soil
than from bare soil following equivalent applications of urea fertilizer to
the two soils. On unfertilized grassland in semiarid regions, some loss of
ammonium nitrogen from the system is known to occur from urea nitrogen
voided by grazing livestock. B. A. Stewart (1 970) found that following
addition of steer urine to bare soil with surface drying conditions, volatilization loss could be as much as 90% of the applied nitrogen. However,
urine-voided nitrogen that becomes volatilized is not necessarily lost from
the soil-plant system. It may be returned to the soil in precipitation or it
may be reabsorbed by moist surfaces (plant, soil) or free water surfaces
within the ecosystem.
This review stems from participation by the authors in the Grasslands Biome segment
of the International Biological Program. Its compilation was supported in part by National
Science Foundation Grant No. GB7824 and in part by the Canadian National Research
Council, being issued thereunder as CCIBP Report No. 41. The authors gratefully acknowledge helpful suggestions and discussion received from many colleagues at the Pawnee
and Matador grassland sites in the United States and Canada.
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