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A chapter from
Adaptation of Chickpea in the West Asia and North Africa
Region
f+p
Edited by
N P Saxena, M C Saxena, C Johansen, 5 M Virmani, and H
Harris
International Crops Research Institute for the Semi-Arid Tropics
International Center for Agricultural Research in the Dry k#r
Patanchew 502 324. Andhra Pradesh, India PO Box 5466, Akppo,
Syrk
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5.5. Symbiotic Nitrogen Fixation by Chickpea in WANA and SAT
D P Beck1 and 0 P Rupela2
Introduction
'I'ht- :ability of i hic.kl)es to lix i~t~riospht~rii. nitrogen
Icssrns its dispcn- dcnce nrr soil N i d rc.inf'orc.cs its rolc in
the cropping s y > t t * ~ ~ ~ s ol WANA and SKI'. 1 lowever,
the crop is oft(-n considrrcd infrrior in this rt.garcl to other. I
C ~ I I I I ) ~ (raps p w n in whmt-biletid rotations (I'upil-
styliani>u 1987; Keiitingt* tat ill. 19HX). P~lhlishcd
cstiti~atcs of N,, fisa- ticln hy uhickpra in the WANA region range
from 0 to 17ti kg ha-1 per scason, with tllr propottion of total N
I'ron, fixatiori virryirlg ht*tween O and 82010, depending on thr
method ot' Ineasurt*mc5nt, i.11lti- KIT, prtsscncc of a ~ ~ ) r ~ t
) r i i l t ~ ' rhix~~biil, and t~nvironrnental variables (IZizk
191i6; I'apastylianou 1987: Kciltinjic ct al. 1988; Hcck ct al.
1991). Nitrogtnn lixation has a positive cl'fect on soil Nz balance
and growth of thc suhscqtrcnt crop (Evilns 1982; Heichcl 1987;
Kcirtingc r t al. 1')HH). 'l'hereforr, prarticivi which inr.rcasc N
fixation will mini- mize t h ~ quantity of sail N utiliwd by the
crop, and therehy incrmsr yields in the subsequent non-legurne
crop.
l'hc main stri~tcgics for improving biological nitrogen fixation
(HNF) in chickpea are similar t o those for most legumes. Btscausr
the process of N, fixation is photosynthate-driven, increasing chir
Lpca yield is thc simplcst and gcncrally thc 111ost successful
strategy to iml~r~ovr RNF. Hrectiing for improved N2 fixation is
rarely done because it gets less priority than that for yield and
resistance to biotic/stiotic strcsscs, and also hrcer~sc mcasrlring
NZ fixation tnay bc a difficctlt and cxpen-
... . ... ,,. I C ~ P ~ I I I ~ ~ ~ I W I I > I ' r t ~ f a l
I ~ ~ lC:AMl>A, I X ) NIX 54iiii, Ah-I~UI. Svrw 2. Agronomy
Dlvr'i~irn. IL'RISATArir Crntcr. I1iltanchc*ru 502 324, Andhra
I'raiirsh, l n ~ t l ~ .
sivc process. 0;)tirrlizlng thr host-rh~zob~,~ ;issot littion,
hv Inoc c~latinc the c.liic.kpc*a pli~nts with \c.lcc tixl
rt,~zolrl;t, I \ ~ t~crr tor i , , tflt* most r.ornnion ;tppri.)ai
h to improvr K,. f~x;~! ion.
'T'cchniqrlc*~ );IT rllcilsurlng S:. fixat~or~ arc* +4s.
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the fixation process (Munns 1977; Streeter 1988). This factor is
par- ticularly important in experiments conducted at research
stations, where soil fertility (N in particular) tends to be
high.
Critical tolerance levcl and degree of suppression vary ~ t h I
w m e species (Harper and Gibson 1984). The limited research on
chickpea indicates that levels of NOsN below 10 ppm will not
adversely affect N, fixation (Rawsthorne et al. 198S), but
variation with cultivars is expected (Rupela and Johansen
1992a).
Chickpea also appears to be a fairly efficient scavenger of soil
N, especially under conditions where sufficient rhizobia are not
present for efficient symbiosis (Beck 1992). The practice of
fertilizing chick- pea with 20 kg N ha,' at sowing is widely
recommended in SAT, probably because it somctimes helps to negate
the adversc effect of high temperature on symbiosis (R~wsthorne et
al. 1985).
Nitrogen fixation in chickpea sectns to be morc sensitive than
grain production and N assimilation (which is mainly limited by
availability) to high tetnpcratures (Hawsthornc et al. 19115) and
drought Wery ct al. 19811). In field studies with six chickpca
cultivars in Syria (ICARDA 1992), drought strcss depressed Yfi,
more than N uptake (Fig. 5.5.1). A line-source sprinkler was used
over 2 seasons in thcsc studies, where Pflx increased more rapidly
than yield at lower moisturc levels, indicating that fixation wes
severely limited at the lower end. Values for Pfi, in different
cultivars at lower moisture levels varied widcly from 15 to 38%.
Fixation efficiency reached an average maximurn of 6896 at about 5
0 0 kg ha-1 dry matter produced. Nitrogen uptake from soil remained
constant until moisture became sufficicnt for max- imum fixation,
when soil N uptake increased (Fig. 5.5.1). Thc correla- tions
between dry matter prodr~ced and N yields were high, with
coefficients of 0.92 for tatal N and 0.90 for fixed N.
The high correlation between dry matter production and N yield
indicates that N, fixation in chickpea, under conditions where ade-
quate rhizobia are prcsent, is yield-driven, and that
cnvironrnental
Q "tis m Total crop N
I 0 Fixctl N
-1 xo 150 0 0 0 0 0
Figure 5.5.1. Relationship of dry matter production with N yield
and source in chickpea cultivars, northern Syria, 1987-91.
constraints on plant yield will limit N2 fixation. These rearlts
may partly explain why N fertilization impraves yield of
nonirrigated chickpea in low N soils, but does not affrct yield in
the irrigated crop (ICRISAT 1992).
Breeding for improved N, Fixation
Agrononiic and cnvironlnental considerations often limit the
biomass yield of a legume crop and therefore the capacity of that
crop to fix
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N,. Yicld is also determined genetically, for example, low N
yield may be a characteristic of somc species. In studies ovcr a
range of environ- ments and agronomic practices, N yield and N,
fixation by chickpea wcrc consistently less than for the other
cool-season food legumes (Rennic and Duhetz 1986; Evans and
Herridge 1987; Snrith e t al. 1987; Beck ct al. 1991). Average
yields wcre 100 kg N ha.' fbr chirk- pea, 196 kg N ha-1 for lentil,
185 kg N ha-1 for tirld pea, and 200 kg N ha-' for fabo bean. These
studies did not indicate that the inherent capacity of chickjxa for
ncdulation and N2 fixation was less than for the other sprcies. It
may be concluded, therefore, that inrrrasir~g N yield of rhickpca
may rcsult in increased N, fixatior~.
Plant breeders select for high yield within the constraints of
local environments and crop yields largely detcrmintl thc amount of
N2 that is fixed by the crop, particularly in low N soils
(Hardarson c-t al. 1984; Kumar Hao and Ilart 1987). Therefore,
breeders who mustly work in low N soils will tend t o sclcrt for
niaterial with RCK)(I capacity for N2 fixation. Hreeding for
symbiotic characteristics in chickpea is possible. Ex;u-nplcs of'
possible strategies t a exploit art. nitrate tolrr- ance (i.c., the
ability ot'the plant to nod~llatc and fix N2 in the prcs- encc of
soil nitrate), the capacity t o fix Nz at low available moisture
Icvels, and general ndulat ion capacity. Chickpea cultivars
sclectcil for cirought tolcrancr seem to vary in their capacity for
N2 fixation under drought stress. Natural variation for nitratc
tolcrancc (Hupcli~ and Johansen 1995) and ntdulation capacity
(Hupcla 1994) also rxist in chickpea. I t may be irr~possiblc to
produce a Icgume that is dcpen- dcnt solcly upon N2 for growth and
cannot use nitrate, but there is scope to improve Pf,, in thc
presence of nitrate for chickpea.
Some argue that legumes should be ohle to tise bc>th
atmospht.tic and soil N sources so that they can scavenge nitrl tr
horn the soil which would otherwise be lost through leaching and
denitrifi~-ation, while others argue that in many soils, nitratc is
relatively stahltp over t ime and can be considered as a stable
pool of N. Secondly, if dcplt*.
lion of' soil nitrate was considered rircessary, i t wol.~ld
make rnore sense t o use D rrreal cmp w ~ t h a highrr tlemand for
N and greater econamlc rrturn.
Recacise N yield and dry rnattcr productlirn art1 gcnrrally h
i~h ly correlated (Mytton 1983), thta f;)lIowiny: proc.c.c.iure
could be followed to enhance N-, fixallon in ch~ckpca:
I . Scrren a large and divcrsc jirrr~ipli~sm (500-IOCW
genotypes) of c.hickpra, inc)c~ihtcti with highly effective
rhlxohia. For production 01' dry mtlttrr uridrr low N conditions
(prcfr*r;~bly in thc field, hut ~t could be donc in a
grrrnhousr).
2. Sclrct silpcrivr genotypes ( c , ~ . , top lo'%,) fur
flirther cvnluatlon. 'The sccond round of' screening is ideally
done In th r f~eld on low N-f'ertility soil, ajiain with a mixture
of h~ahly rf'tectivr rh~zobia. Asscssn~ents should includr
measurements of grain yirld and total N yield.
3. Cotlipare elite grrrotypes over a rarlgr of edi~phic
(particularly soil N fertility) and environmental (including
dlvcrsr rhl~obial popula- tion) conditicrns for grilirj yield, N
yirld, arrd NL, fi~ation, thc latter tising ''IV nlcthcds.
C*;t*notypes that arc identified at this stage RS s ~ i p ~ r i
o r In all three attributes and actepted to the soils and
crrvironnrrnth for which they iilc likely t o bc tised wo~ild h;rvr
a~rmrdratc comxr~crt-ial application. thjih N,,-fixing gtmotypes
that produce low grain yields or grain of low quality could hc
rised as donor parents in a brrrdlng prngrdrrr.
It is also important to rcmovc t l ~ r vff~~i- t of crop
duration un N yield. Increased N yirld due LCI high gcr\\-th and ~
s s i ~ n i l ~ t i i r n rates is nwre uscftll ht.catlse it rean
bc rsprt.ssc*~i in any ~ r ~ v i r o n ~ i l ~ n t ; whcrcas
incrcastd cmp N ciur t o Icinger crnp iiur,rtirtn ~,;ln rrnl!. he
esprcsscd if thc dur i~t i i~n crf the scascrn in 3 parti&-uldr
cnvirnnment or ~.ropping system is suffic.it*ntly Iona. In
cvmmer~.1;11 agri~.\llti~rt, individual crops 111ust fit into
cropping systcnrs \vtiir.h arc rit.tcrlliint*d hy seasc3nal
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clianges in tctnpcraturr, moistt~rc availability, ri~diation,
i~voilahility of' land and rcsotlrccs to grow and harvest thc crop,
n~arketing nrringr- ments, etc.. 'The optitilurn driri~tion of' any
crop is thcrcfure dctcr- mined hy several f i~~tors, tlic. least
important of whir11 is N yirlii or N;, fixatiorr.
Inoculation
lacal production or itnport ol' inocr~lants for i'armrrs can
only be justified if thc* Ity,unic benetits from inoculation ilrr
showr~ by in- crcilses in yicld or it\ N, fixation in tirld trials
ancl hrmrrs' fields. It is essential to detcrrrrint* thc need for
inoculation before initiating any program on inoc~lilrlt
dt*vrloptllmt, production, distrihr~tion, or usc. Response to
inoculation by Iegun~cs has hrcn shown to he influcnccd mainly hy
cropping history (Rrockwrll cr al. I!)HZ), soil N :ivailahility
(Somascgaran arid Rt>hlool 1900), and most important l y, tlic
indigc- nous popr~liltion of rllizohia that nodcllate thc host
(Thies et al. 1991). Various methods to dctcrrninc the need for
inoi-ulatiort arc. describcd in detail by Beck ct al. (1993).
'Thc introdt~ction of cold-tolcrunt, ascochyta blight resistant
lines for wintcr sowing into new, drier production arcits of WANA
has been accon~~anicd by nodtilation dcfic.iency in scvcral arcas
(M Solh snd S P S Hrniwal, personal co~nmunication). In these new
production areas, soils are lcss likely to contain adequatc
populations of the C'iccr- spccific rhimbia than traditional
c:hirkpea arcns, and crops tnay show significant yield incrcascs
when seeris are inoculated with selected rhizobial strains.
Extensive surveys of native r11i;~obia-nodulating chickpca have
been reccntly conducted in Syria and Turkey, where symbii>tic
effectiveness and size of native populations wcre measured
(Kcatinge et al. 1995). It was found that even within the major
chick- pea-growing regions, many soils contained rhizobiel
populations eithcr at very low levels or with low symbiotic
effectiveness on the cultivars
tested. It has h e n sr~ggested that this deficiency may bc one
rcason for the grncrally low average chickpea yiclds from these
arcns.
The highly specific rtli~uhial requirement of chickpea extends
to strain-cultivnr specificity for N2 fixation (Beck 1992). This
inlplics that limited cffcctivcness of naturali7td rhimbial
ppulations with nrwly introdt~ced ctlltivars may restrict the
genetic potential for di- nitrogrn fixation. Nwcssity for
inoculation may therefore also exist where introduc.cd cultivars-
-selrcted for high yiclds-cannot express their ftlll capability for
N2 fixation in symbiosis with native rhizobial populations that
hove devclopcd in aciaptution with Iwal Iandrarrs.
In trials conducted over 4 scasons (1987/88-1990/91) in northern
Syria (seasorla1 rainfall of 300-51K) tnm), variations in N2
fixation and yield of chickpcn cultivars inocttlated with srlccted
Rhizobium strains wcrc evalllated. 'l'hc purposc was to establish
base-line valucs for PI; , in recor~~rnendcd cultivnrs so that
improvements throt~gh rhimbial strain selectiori and lcgume
breeding could be quat~tified. IJsc of 1 S N methodology and
nonnodulating chickpea and barlcy as refcrencr crops allowcd
accurate evaluation of N2 fixation tmder a wide rangc of
cnvirontnental conditions. Indigenous chickpcu rhirnbial
popt~lations based on the most probable number (MPN) estimations in
the field soils were low to moderate, ranging from 9.1 x 10' to 4.2
x 10" rhimbia g-I soil. Rhi.u>bial strains wcrc se1et:ted
according to the N2- fixing perfonnancc in aseptic hydroponic
culture in greenhouse trinls.
Inoculation had no general cffect on crop dry rnatter yields at
lower rainfall sites (Pig. 5.5.2). At 340 mm rainfall, however,
crrltivars began to show differential yield effects with rhizobial
inoculation, ranging From no response to n 750 kg ha.' increase.
IJnder conditions of higher moisture (504 mm), thc averagc
inoculated cultivar yiclded about 800 kg ha-1 more dry matter than
when not inoculated (Fig. 5.5.2). Cultivar yields, which differed
little at low rainfall, varied widely at high rainfall; yield
rcsponsc to inoculation varied from no response in cultjvar ILC:
5396 to 1.9 t ha-1 in ILC 482.
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N tutal inoculated 0 A N total uninwulated o DM yield inoculated
m DM yicld uninoculukd A N fixcd inoculated v N fixed uninoculated
+I
Annual rainfall (mm) Figure 5.5.2. Effect of inoculation on dry
matter production and N yield in chickpea, norihern Syria,
1987-91.
In uninwlated cultivars, PC, rcmains rclativdy constant at about
GO'% between 2000 and 7001) kg ha-l dry matter production (Fig.
5.5.3). The effect of this constant proportion of fixed- to
soil-derived N in the plant is that with increasing dry matter (and
N) production, the quantities of soil N taken up by the crop
increase. Fiyrr 5.5.3
shows average soil N uptake (the distance bctwcen total N and
fixed N curves) increasing from 20 kg ha-1 to nearly 50 kg ha-1
over the range of dry matter produced in the trials. In contrast,
the efficiency of NZ fixation has clearly increased at higher yield
levels as a result of rhimbial inoculation (Fig. 5.5.4). In
inoculated cultivars, Pflx increases with dry matter production,
reaching a maximum of 80(#1 at the high- est yicld Icvels.
Increased fixation efficiency with yield results in a high
proportion of fixation-derived N in the plant and a low, relatively
constant fraction of soil-derived N (Fig. 5.5.4).
1.k: 1!1,11lc*r \ tc l~ l (kt! h.1 ' Figure 5.5.3. Nitrogen
yield and source in uninoculated chickpea cultivars, northern
Syria, 1988-90.
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I I I Ittin) ?(nu\ .zcnn) 4 n w ) s t n u ) o c r n ) 'Itnu)
ntnn,
IJr) ~ i i : ~ t t \ - ~ ~ ~ r t ~ l u c t ~ ~ ~ ~ ~ ( k g I1i1
I )
Figure 5.5.4. Nitrogen yield and source in inoculated chickpea
culti- van, northern Syria, 1988-90.
In mast cultivars tested, inoculation did not increasc the
amount of crop N per unit dry rnattcr produced. The proportion of
crop N derived from fixation was, however, often increased by
inoculation. The effect of this impravcment-that can be detected
only with N, fixation mcasuremcnt techniques such as thosc
incorporating 'SN-is improved soil fertility. Although the cffccts
of inoculation on yicld arc limitcd, the quantities of soil N
preserved could be significant in a systems context. Farmers,
howevcr, will not adopt inoculant technol-
ogy it' they do not get as a result of applying the technology,
increa.wd yiclds ot' thc legume or ol' thc subsequent c.crral
crop.
The itrterat:tion ktwccrr strains and rultivars for N2 fixation
effi- cicncy, in addition to a similiir interaction Ihr
cor~ipetitiorr and nodule formation, coniylicates the approach t o
wide-scalc intwulation of chickpea cultivars, csyccially wticre ncw
improved cultivars arc being rcleasrd on a rrgulur basis. Two
strategirs triay hc used to increasr N fixcd hy tlic chicklwa crop.
Sclecrion of cultivars for high N;, fixation with a broad mnge of
rhiwbia rcduccls the nerd for inoctrlation with specific strains.
'l'liis, howcvcr, may fail whcrc nativr strains arc absent or
incffcctivr. Alternativrly, mixtures of highly effective strains
may hc used as inoculants. This works with some cultivars, but is
dcpcn- dent on strain-cultivar interaction for competitiveness in
nodule for- mation, and on tho sucr:essfttl use of inoculant
technology by farmers.
Evvm whcrr ir~oculatio~~ can irrcreasr yiclds, its ellictivcness
is heavily dctwndent 011 the qt~ality of the inoculant and the way
the prt)dt~ct is apl~lird. Exprriencr has shown that successful
transfer of i n t ~ d a n t tcchnology to farmers for improvement
of BNF is difficult at bcst (Thompson 1991). Rhiznhium incwulants
arc biologiral produrts and thrrcfore s~rsceptiblr to major
problcms with ~nanufacturing (quality control), distribution (loss
of viability during transport and distribution), and extension
(Roughley 1988). Slistribution of poor quality inoculants is not
uncommon, and is g~ncrally followed quickly by fanner disinterest
in inoculation.
Contribution of N, Fixation to Cropping Systems Results from
legume-bascd rotation cxperimcnts in rainfed cropping arcas of many
countrics havc been published in recent years (e-g., Evans and
Taylor 1987; Evans a al. 1989). 'fie* cxpcriments reflect the
growing concern of scientists and farmers in thosc areas about
declining levels of N fertility in the soils and rrduccd production
of
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tion and its valt~c t o soil N incrcascs in lupin, field pca and
other legumcs in south-eastern Australia. Australian Jot~rnal of
Agric\~ltwol Rcscarch 40:791-805.
Evans, J., and Taylor, A. 1987. Estimating dinitrogen (",I
fixation and soil accretion of nitrogen hy griiir~ Ichwmcs.
.lournal of the k ~ s t r a - linn Institute of Agrirulturnl
Science 53:78-82.
Hadarson, G., Zayata, P., and Danso, S.K.A. 1984. Effects of
plant genotypes and nitrogcn fertilizer on symbiotic nitrogcn
fixation by soyhean c~lltivars. Plant and Soil 82:397-405.
Harper, J.E., and Gibson, A.13. 19H4. 1)iff'crential ntdulatiorr
toler- ance lo nitratr anlong legume slxcics. Crop Science
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Hrirhel, G. 1987. I.rgumr nitro~en: sytnbiotic fixation and
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Peoples, M.B., Vaizoh, A.W., Rcrknsc:ni, R., and I lerrid#e,
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irrtrnsivc i ~ o p -
I-urbl: in thr, tropic.s c~n(.l s t~h - \ rop~ i , \ , ~ j r i ~
t,*c.c.l~nq\ ot t l ~ t . Intcsr-( (lrl:!r(*\\ (:r)nl'c.rt~nt.c! 1
1 t C:onlrnls\ion IV, 1-3 TI(.( I ~ I I , I ~ , I ,
lL~r\~!liu!f-,t~ (1 IIISS:IIII, ,M.S., IIII,IIIIII! 11~11, !- ,%I,
, /Int\.,lr Iqlr,11, A!., , I ~ I I ~ Kl.~:lr:, ' I . I I (*(Is,].
IIhakii, N;lnt:l,1tlt4i: l l .~rri :I , icl t~\t i 1I2r1i I I I ~ I
. I T ; I I I ~ i * ~ c ~ r ~ r t i : (. : o1111r 1 1
S:lxcbrte, M.(:., Silim, S.N., ,rrrcl Singh, K.13. I ( + l ( r
1:ttt.i I c ~ f \itpplta. rTIC1ltilry irrigiitlo~l cluring r t ~ l
) r ~ ~ ~ l ~ ~ ~ . t i ~ t ~ c r o ~ . : l ~ t)n \ \ . ~ r i ~ t ~
r \111i.i ! I I I 07:3-. 13.
Sor t ln s r~ i tn~n , P., ;lnd Rohlool, H.M. I i I ( d ( I
C;inclt-.~tra~r: : ( * I -1.1. 1n11lt1 stri~in II IOC ~ ~ l i ~ t i
r m : i4fi*c t of soil I I I I ~ I : ~ , I ~ S ~ ~ ~ , i i ~ . ~ l
~ i ~ ~ t ~ . t t r r r l i i~ r~ l>~a l Strillrl i $ l l ~ i
tivcrlinh\ ill^! ii S,. f ~ s a t l o r l by rritrirtc. ( :riili
ill Kc\ it.\\.!- 111 Plant Si.~t*llt t o -:I : !
'Ihics, .l.E., Singleton, I".\\'., ;1111l Bohlool, H.U. lt.)'!1
I r i t l ~ r ~ ~ n i t s ijt tlrc ~1x1: ot' i r ~ i i i g r n i )
~ ~ ~ rhiLirbl.tl pirp~rI;~trorr\ tjn t.>t.lhl~shr.ncnt :irlri s
~ ~ r l h i i j . tii. pc.rt;irrnanc.t. (if' ititrodur~i~tl
rh~zc~hi;i vrl tli.lcl.~:r(j\vrl I ~ * ~ \ I I I I c ~ ~ . A!)-
pliivl Errviron~rrct~ti~l X l i k r v h i i r l o ~ .?-:
19.-75.
' f ionipson, .l,A, l!)!ll. l , t * g ~ ~ ~ i i t ~ i n i ~ l -
~ ~ l ~ r ~ t l i r i x l i ~ t ~ t ~ ~ ~ n ;~ tx i ~111.1ltt\, t t
~ i - tri11. PagcsI15 32 ill Espcrt i .c)nvll t ,~t~o~i ern I t - p
~ ~ r r c Inoc rll'rnt I>r , t l~ lu~. . titrn irnd r l t~a l~ty
~ .unt ra l , Htwtlc*, It,lly: FnoJ .ttlrl 4grir,ultirrt*
0rgnrriz:ltion of thc I inltcd N.1ticln5.
M'c*ry, J., Desc.hurrrps, hi., ; ~ n d I~lgrr-C:'rcsstm, 6.
1!1$S. 1ntlucnc.c vt somc agroclimiitir fdLtors .irlil
dglc~lli~llllr' pr~itit.t*h on nitrogen nutri-
-
t i c z n c > f c h i c - k p r - a ( C i c . - e r
arirrtinum t .-). P a g ~ s 2S7- 30 1 in N i t r r > g c n
fixation by I r g u r r ~ e s in Mcciitrrrst-rran ; r g r i s . . t
r l t t a r t - CBccrk , i-3.1'.. and M a t e - r o r r , 1,-A.,
t-ds-), ' l ' l r c H r a g x r c , N e t l x e r l a n d s :
Martinus Nijho+f-/13r W Junk I ' u l > l i s t r c r s .
W i a a y , J-t:, l9S3- E n t . i x x r a i i t r g N;, f i x a
t i c y n i t - thc - field using 'SN-labcllcd fe-rtil izx-r: s c
> r x ~ c - ~ - r c > l > l c - ~ ~ ~ s ar1r-4 s r > l
~ a t i c ~ n s - S o i l E&ic>lc -gy and 1 % ~ - c - l a c
- m i s r r y 1 5 z f 5 3 1 - 639- Wirty, J,12,, and Minc:hin,
Iz,K, 198s- Mt-asurc'anc-nt 4-1' n i t r o g e r r fix;*- tion by
the a c - e t y l c t ~ r = r r d x s r - t i o n irssay: z n y t h
s R ~ C I rnystc-rics- Pages 3 3 1 -344 im N i t r c ~ g t - r - f
i x a t i c - n by l c g u t n l - s i n M c d i t c r r a n r a n
a g r i c x s l - ture ( H e c k , L3-I)., a r a c i M a t r r r m
r , LA. , c * c t s . ) . 'l'hr- 1 lsgnc, Nrthcrlands: Martin~rs
NijhofT/ I 3 r W Junk P~rhlishtrrs.
Witty, 1 , Rennie, R-J-, a d Arkins, C 3 - A - 19SH. N addition
r r > c t h o d s f i x assc-ssing Nz fixation under f ie ld
c:-nndirions. Yagcs 7 1 S- 730 in World crops: c o o l s c a s r -
n f c x d 1 e g u r x . r e - s CSumn~t-rfic-ld, R - . I - , ed-).
L 3 o r d r e ~ - h t , Netherlands: Kltawer Acadcmir P x a b l i s
h r r s .
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