Soil Bid. Biochem. Vol. 29, No. 36, pp.

771-774, 1997
(r7 1997 ElsevierScienceLtd. All riehts reserved

Pergamon

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BIOLOGICAL NITROGEN FIXATION IN THE TROPICS:

SOCIAL AND ECONOMIC CONTRIBUTIONS
JOHANNA
EMBRAPA

DBEREINER

- Centro Nacional de Pesquisa de Agrobiologia (EMBRAPA-CNPAB),

Km 47,

Seropdica, Itagua, 23851-970, RJ, BRAZIL

(Accepted 4 July 1996)

Summary-Brazil has become the world leader in replacing N fertilisers by biological NZ fixation
(BNF). Even though agriculture in Brazil is one of the main export-producing activities, it has
become the country which uses the lowest N applications (mean 10 kg ha-). Soybeans selected
with zero N applications have become the countrys largest export product. Cereals, also selected
with N supplies much below their need, unknowingly were selected for associations with diazotrophic bacteria and can obtain up to 30% of their N from BNF when fertilised with ample PK
and minor elements. The largest effect in this group was obtained with sugar cane, which can
obtain up to 150 kg N ha- from BNF. This has become the key to the success of the Brazilian
Bio-fuel programme where because of increases in the energy balance when the cane is planted
without any N fertiliser and without buming the leaves, the energy produced is more than 5
times that required to produce it. Recently possibilities of expanding this biofuel programme to
diesel oil are arising from the isolation of probably new diazotrophs which colonise the sterns of
oil palms, of the Brazilian palm genotypes which usually are not fertilised with N. 0 1997 Elsevier
Scieice Ltd

INTRODLKXION

THE BRAZILIAN LEGUME CROPS

in the tropics might be expected to be

more dependent of N fertilisers than that in temperate regions, because heavy rains and more rapid organic matter decomposition lead to leaching and
rapid losses of the N fertilisers applied. In addition
to ground water pollution, other problems due to
high N fertiliser applications occur in the tropics.
High N fertiliser prices, especially in Brazil where
they are not subsidised, can make agriculture
unprofitable. Due to this, plant genotypes have
been selected for high yields with low N fertiliser
applications thus leading to crops which produce
relatively high yields with low or no N fertilisers.
Table 1 gives an overview of the fertiliser applications in various representative countries in the
World.
It can be seen that among al1 countries in the
world, Brazil applies on average the lowest N fertiliser doses. This is not, however, due to fertile
soils, because most soils in Brazil under agriculture
are very N and P deficient as are most tropical
soils. It also is not due to the large areas available
for agriculture, but mainly to the high prices of
these fertilisers here. Low fertilizer application has
not only made agriculture
more economically
viable and competitive in the world, but it has
also reduced groundwater pollution problems turning Brazil into one of the least polluted countries
in the world.

When soybeans were introduced into the country

in the 196Os, adaptation and selection of genotypes
of this crop were made with relatively high P, K
and minor element applications, but with zero
nitrogen added. Consequently Brazil and Argentina,
where our soybean varieties are used, became the
only countries in the world to obtain high yields of
soybeans with absolutely no N applications. Mean
yields in Brazil are now more than 2 t ha- and the
total yield on the 12.5 million ha planted with this
crop make up 25 million tons per year worth 5.7
billion US$. With an N content of 6%, most of
which comes from N2 of the atmosphere, this is
equivalent to 150 million t of nitrogen valued at 1.6
billion US$. Since nitrogen fertilisers have to be
applied at rates twice the amount plants take up,
the economy of the Brazilian soybean crop amounts
to 3.2 billion US!! N fertiliser economised.
Beans (Phaseolus vulgaris) the main protein
source of the Brazilian people, yield on average
600 kg ha- with inoculation used only in part of
the country. Selection of more efficient and competitive Rhizobium strains and bean genotypes could
increase annual yields to 1500 kg ha- with 4% N
equivalent to 375 million US$ (Hungria and Neves,
1988).
Many other legume crops have potential in
Brazil, such as peanuts, and forage legumes, which
contribute to the economy and are partly respon-

Agriculture

771

772

Johanna

Table

1. Fertiliser

applicatmns
m the World
Adubos. 1988)

Country

NPK

Europe
China
USA
Mexico
India
Brazil

335
142
105
63
46
51

172
x7
58
36
27
10

(kg ha-)

(Solos

Dbel-emer
e

NP
13
114
5.
7 h

70
IJ

sible for the low N fertiliser inputs in Brazihan agriculture. The centra1 highland savannahs of Brazil.
called Cerrados, have been partly transformed
into
highly productive agricultural areas with the cultivausing inoculants
specifically
tion of soybeans,
selected for these regions (Botelho (12ul., 1988; Scotti
et al., 1988). If the whole cerrado area (210 million
ha) were planted with soybeans,
enough protein
could be produced to feed one third of the worlds
population at U.S. standards (100 g protein dd).
New projects of reforestation
with legume trees
inoculated
with species of selected rhizobia
and
mycorrhizal
fungi, and grown before transplantion
in to the field in bags containing
50% rock phosphate, apply an additional very important
technology to enrich eroded soils with N and organic
matter (see paper of Franco CJIcl/.. this symposium).

NITROGEN FIXATION IN CEREALS AND FORAGE

GRASSES

Since nitrogen
fertilisers are not subsidised
in
Brazil, most genotypes, and subsequently
commercial varieties, of cereals have been selected for high
yields with N fertiliser rates much below their real
requirement.
This unconsciously
favoured varieties
which obtain part of their nitrogen from associations with diazotrophs.
Initially this was attributed
to rhizosphere
bacteria, but it seemed ditlcult to
explain that as much as 20 to 4006 of plant N
could be supplied by such associations.
During the
last decade, however, it became clear that such genotypes are colonised endophyticalfy
by various diazotrophs (Dbereiner,
1992). some of which have
Herhaspirillum spp,
not
yet
been
identified.
Burkholderia spp and certain strains of Azospirillum
spp have been shown to colonise roots, sterns and
leaves of maize and, Pennisetum and even of Cs
plants such as rite (Boddey et al., 1995; Baldani et
and wheat (Baldani et ul.,
al., this symposium)
1986, 1987). Programmes
of selection of maize and
rite genotypes for high contributions
of these diazotrophs promise good chances of success (Blow and
Dbereiner,
1975A; Toledo. unpub. Ph.D. thesis
1996).

ENERGY

CROPS

Progress made in al1 areas of biomass

been much greater per unit expenditure

energy has
than pro-

gress achieved
in the pursuit of nuclear fusion
(Rosillo-Calle
et al., 1994). These authors suggest
that if half of the money spent in the world on
nuclear energy had been applied to the study of
bio-energy alternatives,
large amounts of renewable
energy sources would have been developed.
The elimination
of N fertilisers for bio-energy
crops represents a major key to high energy balances. The Brazilian ethanol programme is the best
example of this (Dbereiner,
1994). Sugar cane
grown in the country for centuries never received
high N applications
and therefore
the genotypes
developed and grown today obtain the highest BNF
contributions
among al1 non-legumes.
When grown
with ample P fertiliser and foliar applications
of
molybdenum.
this
crop
can
obtain
up
to
150 kg N ha- year from BNF (Urquiaga
et al.,
1992). Sugar cane is now planted on 4.2 million ha
in Brazil, 8% of the land under agriculture.
With
mean yields of 64 t haar, in addition to sugar, 14.2
billion litres of ethanol
are produced
per year,
equivalent to 260000 barrels of petrol per day. Four
million cars run on 80% ethanol, and al1 gasoline
sold in the country contains 20% absolute ethanol.
Even though petrol prices over the world are currently low. the government
is convinced
of the
social and ecological impacts of the biofuel programme and plans to support it further. The key to
this program is the high energy balance which is
shown in Table 2.
Due to the high N contributions
certain sugar
cane genotypes
receive from BNF, we are now
recommending
that farmers plant this crop without
any N fertiliser and use the funds otherwise used
for N fertiliser for increased phosphate applications,
foliar spraying of Mo solutions
(0.5 kg Mo ha-)
and irrigation.
Elimination
of leaf burning before
harvest, in addition. increases soil fertility and the
soil cover from plant residues reduces needs for irrigation.
The
higher
labour
need
for cutting
unburned sugar cane provides more jobs and costs
are compensated
by further
increased
yields
(Oliveira er ai.. 1994). The Pro-alcool
Programme
has already created more than one million jobs and
Table 2. Energy balance of ethanol production
Brazil (Boddey, 1993)
Mean crop yields
Mean ethanol ylelds
Energy produced
Ethanol
Bagasse
Total
Energy expended
Agriculture
Factory
Energy gain
Overall energy balance
Energy balance assuming
derived from bagasse
Eoergy balance assuming
applicatlon

from sugar cane m

65 t ha- yr-
3564 L ha- yr-
18.747 Mcal
17.500 Mcal
36.297 Mcal
4.138 Mcal
10.814 Mcal
2 1.345 Mcal
2.43
all factory power
zero N fertiliser

4.53
5.79

113

Biological nitrogen fixation in the tropics

could be further increased, thus helping to solve

one of the major problems of our country, the
over-population in the main cities. Elimination of
cane buming also wil1 further reduce air pollution;
use of fuel alcohol has already reduced the lead
content in the air of the large cities by 75%. Motor
cars running on alcohol also emit 57% less CO,
64% Iess hydrocarbons and 13% less NO, than
cars running on gasoline.
POSSIBILITIES

FOR THE REPLACEMENT

FUEL

OF DIESEL

In addition to the alcohol programme, possibilities are being studied by Petrobras, the Brazilian
state-owned oil company, to replace 20% of diesel
oil by palm oil. Oil palms in Brazil are grown in the
poorest North East area and in the Amazon
regions, but Brazil is one of the tropical countries
which produces relatively little palm oil, only 0.6%
of world production. There are large areas available
where oil palms could be planted, and it has been
estimated that 18% of this already-deforested area
could produce sufficient oil to replace al1 diesel oil
used in the country (460000 barrels d-) (Oliveira,
1985; Boddey, 1993). Planting costs are relatively
high, but harvest costs are very low; harvesting is
by hand and mules are used for transport. These
areas could be reforested with legume trees mixed
with oil palms, and this would not only help to restore the Amazon forest but also would create important income for the poor Amazon population
without causing environmental problems. Oil palms
can be harvested continuously throughout the year,
and the fuel can be processed by simple pressing.
This leaves much less residue than other biofuel
production
systems. Among al1 liquid biofuel
alternatives oil palms produce the highest amount
of energy ha- followed by bio-ethanol from sugar
cane (Table 3). Among the different oil-producing
crops, the oil palms (Elaeis guianensis and Bactris
produce the highest oil yields ha-], 10
gasipaes)
times more than soybeans or rape (Table 4).
Investigations on growing palm trees without N
fertilisers, showed insignificant responses to N fertiliser by genotypes planted in Brazil (Chepate et al.,
1988). This is apparently
because oil palms have
always been planted in the poor Northeast and

Amazon regions where no N fertilisers are used.

Based on this, we recently started to search for
Table 3. Energy yields of the most productive
(Dbereiner et al., 1981)
Yields
(t ha- yr-)
Oil palm
Sugar cane
Mank
Sweet sorghum

35-38
60-90
13-40
35-50

Equal to 10 Kcal ha- yr-.

biofuel plants

Fuel L ha- yr- Energy TOE

3780
4020
2340
1925

3.7
2.1
1.2
1.0

Table 4. Oil and energy yields of different oil crops (Purseglove,

1968)
Plant

Growth period
(days)

(t ha-) Oil

Energy TOEa

365
365
165
150
120

4.0-8.4
4.8
1.5
0.7
0.6

3.1-7.8
5.7
1.8
0.8
0.7

Oil palm
Pejibaye
Coconut
Rape
Soybeans

Equal to 10 Kcal ha- yr-.

their source of N and found about 106 diazotrophs

g- fresh weight of roots, sterns and leaves of both
oil palms and pejibaye. Herbaspirillum,
Azospirillum
amazonense
and some apparently new diazotrophs
were isolated from these trees, and even the seeds
of the palm trees contained the bacteria within the
endosperm, suggesting how they are transmitted
(unpublished data from our laboratory).
These findings fumish an excellent basis for
exploring the use of palm oil for partial or even
complete replacement of diesel oil. In the poor
northern regions of Brazil, large areas of oil palms
could be planted in mixed forests with legume trees
and thus rejuvenate eroded deforested areas with
good profits for the local populations. This practice
could then be extended to other tropical countries,
primarily Africa, where the cultivation of oil palms
has recently been decreasing.

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