Nitrogen uptake from 15N-enriched fertilizer by four tree crops in an Amazonian agroforest

12 Pages·2003·0.57 MB·English

Agroforestry Systems 57: 213–224, 2003. 213
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
Nitrogen uptake from 15N-enriched fertilizer by four tree crops in an
Amazonian agroforest
Harald Dinkelmeyer1,2, Johannes Lehmann1,3,6,*, Andreas Renck1, Lucerina Trujillo4, Jose
Pereira da Silva Jr.4, Gerhard Gebauer5 and Klaus Kaiser1
1Institute of Soil Science and Soil Geography, University of Bayreuth, 95440 Bayreuth, Germany; 2Institute of
Geography, University of Erlangen, 91054 Erlangen, Germany; 3Federal Research Institution for Forestry,
21027 Hamburg, Germany; 4Embrapa Amazonia Ocidental, 69011-970 Manaus, Brazil; 5Institute of Plant
Ecology, University of Bayreuth, 95440 Bayreuth, Germany; 6Department of Crop and Soil Sciences, Cornell
University, NY 14853 Ithaca, USA; *Author for correspondence (e-mail: [email protected]; fax: (607)
255-3207)
Received26March2002;acceptedinrevisedform6October2002
Key words: Humid tropics, Nitrogen competition, Nitrogen leaching, Root activity, Stable N isotopes
Abstract
Mixedtreecroppingsystemshavebeenproposedforsustainablenutrientmanagementinthehumidtropics.Yet,
thenutrientinteractionsbetweenintercroppedtreeshavenotbeenaddressedsufficiently.Inthepresentstudywe
compare the temporal and spatial patterns of the uptake of applied 15N by four different tree crops in a mixed
tree cropping system on a Xanthic Ferralsol in centralAmazônia, Brazil, during one year. Most of the N uptake
occurred during the first two weeks. Very little N was recovered by peach palm (Bactris gasipaes), more by
cupuassu (Theobroma grandiflorum) and annatto (Bixa orellana) and most by Brazil nut (Bertholletia excelsa).
Due to tree pruning the total accumulation of applied 15N in the above-ground biomass of annatto decreased
throughout the year. It remained constant in cupuassu and peach palm and increased in Brazil nut. Brazil nut
showed an extensive root activity and took up more fertilizer N applied to neighboring trees than from the one
applied under its own canopy in contrast to the other three tree crops. Therefore, trees with wide-spread root
systems may not need to receive N fertilizer directly but can take up N applied to other trees in the mixed crop-
ping system. This means that such trees may effectively decrease N leaching when intercropped with trees that
have dormant periods or places with low N uptake, but also exert considerable resource competition.
Introduction treecropswithperennialrootsystems,largelossesof
fertilizerNfromthetopsoilwereobservedwhichac-
High precipitation leads to rapid water percolation in cumulated as adsorbed nitrate in the subsoil (Schroth
central Amazonian upland soils (Rozanski et al. et al. 1999).
1991).Additionally, these Ferralsols are strongly ag- Acombination of different trees may reduce these
gregated (Lehmann et al. 2001a) and are therefore losses because growth cycles and root activity distri-
highly permeable. Due to high weathering they have bution of different tree crops may complement each
lowexchangecapacities,andnutrientretentioninthe other (Schroth et al. 2001). This would lead to a
topsoilisconsequentlylimited(VanWambeke1992). higher use efficiency of applied fertilizer and reduce
As a result, high leaching losses of applied fertilizer leaching losses. On the other hand, competition for
were observed, e.g. under maize in the centralAma- nutrients may decrease the production of one crop or
zon(Cahnetal.1993;Melgaretal.1992).Treeswere the whole system.
reported to reduce nutrient leaching in comparison to Nutrientinteractionsbetweentreesinmixedcrop-
annualcrops(BureshandTian1998).Butevenunder ping systems are difficult to determine due to their
214
complexgeometries.Assessmentoftherootdistribu- Spreng.) K. Schum. (cupuassu), whose fruit is used
tioncangivevaluableinformationaboutthearchitec- for juice and ice cream; Bactris gasipaes Kunth.
ture of the belowground biomass, but often fails to (peach palm), for heart of palm production; Berthol-
quantify short-term dynamics of nutrient uptake.Ad- letia excelsa Humb. & Bonpl., producing Brazil nut;
ditionally, trees in tropical lowlands may have very Bixa orellana L., an important local dye (annatto),
deep root systems (Canadell et al. 1996; Nepstad et andalegumecoverofPuerariaphaseoloides(Roxb.)
al. 1994). Because of the low root abundance in the Benth. (pueraria). Cupuassu and Brazil nut were al-
subsoil, determination of their contribution to total ternately grown in the same row with a distance of 7
nutrient uptake is difficult. Tracer studies can help to m. In the adjacent rows at a distance of 4 m either
quantify these spatial and temporal patterns of nutri- annatto (4 m distance within the row) or peachpalm
ent uptake (Lehmann and Muraoka 2001). Therefore (2mdistancewithintherow)weregrown(Figure1).
we used 15N-enriched fertilizer to compare the dy- The rows on both sides of peach palm and annatto
namics of N uptake by four intercropped trees on a were planted with cupuassu and Brazil nut; therefore
Xanthic Ferralsol in the central Amazon during one peach palm and annatto did not neighbor each other.
year.Thepurposeofthisstudywas(i)tocomparethe Fourplotsof7×8masshowninFigure1wereran-
spatial distribution of N fertilizer use; and (ii) to de- domly located in blocks with the dimensions of 48 ×
scribe the temporal dynamics of N uptake by differ- 62 m and replicated three times (randomized com-
ent tree crops in anAmazonian agroforest. pleteblocks;totalamountofplots=12).Plotswithin
ablockwereseparatedfromeachotherbyatleasttwo
rows of trees (12 m) to avoid cross contamination.
Materials and methods Peach palm was managed for palmito production
(heart of palm) and cut every four to five months.At
The study was carried out at the Empresa Brasileira planting pueraria was sown between the trees and
de PesquisaAgropecuaria (Embrapa)-Amazônia Oci- manuallycutunderthetreecanopyeverythreetofour
dental29kmNorthofManaus,Brazil(3°8(cid:1)S,59°52(cid:1) months.At the time of this study, pueraria cover was
W, 40–50 m above sea level), in 1998 and 1999.The stronglyreducedduetoshadingandverylittleground
rainfalldistributionisunimodalwithamaximumbe- vegetation was present. Nitrogen uptake by pueraria
tween December and May (211–300 mm per month; and ground vegetation was presumed to be low and
75% of annual rainfall) and a mean annual precipita- was therefore not quantified. Fertilizer applications
tionofabout2100mm(1931–1960;Rodriguesetal., weresplitequallybetweenthebeginningoftherainy
1971,unpublished;andRibeiroandAdis(1987)).The seasoninDecemberandtowardstheendoftherainy
vegetation is a tropical lowland rainforest. The soils season in May using 95, 42, 85, 42 g N (as ammo-
are Xanthic Ferralsols (FAO 1990) and derived from nium sulfate) per plant and year for cupuassu, peach
Tertiary sediments. They are very deep and clayey, palm, annatto and Brazil nut, respectively. Dolomitic
withlowpH(inH O;4.0–4.5),mediumlevelsofor- lime and Atifos (North Carolina Phosphate, 13% P)
2
ganicC(18.9mgg−1)andN(1.6mgg−1)butlowin was broadcast on the soil surface at a rate of 1.9
Pcontent (6.3 mg g−1), cation exchange capacity (21 Mg ha−1 and 19 kg Pha−1, respectively, in 1996. By
mmol kg−1)andbasesaturation(33%)(alldatafrom the start of the presented experiment, the trees were
c
a 7-year-old fallow within the present experiment (n six years old and in full production apart from Brazil
= 3); Schroth et al. (1999)). nut.
Duringtheexperimentalyear,theregularfertilizer
Experimental setup applicationwasdelayedbyafewweeksduetoalate
start of the rains. On 12/13 January 1999, 15N-en-
The site was first cleared in 1980 for a rubber plan- richedammoniumsulfate(10atom%15Nexcess)was
tation (Hevea brasiliensis (Adr. Juss.) Muell. Arg.), addedtoonlyoneofthefourtreespeciesineachplot
which was abandoned in 1986. The developing sec- using1g 15Nexcessperindividualtreeresultingina
ondary forest was cut and burned in 1992 in order to total 15N application of 1, 1, 3, 4 g 15N per plot to
establish several cropping systems mainly with fruit Brazilnut,cupuassu,annattoandpeachpalm,respec-
trees during the first half of 1993. Here, we investi- tively(Figure1).Inanyofthefourplotsonlythefer-
gated the uptake of N in a multi-strata agroforestry tilizer applied to one tree species was labeled,
system with Theobroma grandiflorum (Willd. ex whereas the other trees only received unlabelled N
215
Figure 1. Spatial layout of the experimental unit (I., values denote distances between trees in [m]) and application of 15N (II., distances
betweenplotsnottoscale)tofourdifferenttreecropsinthecentralAmazon;signaturesfortrees(A–D)correspondtosetsofdatashownin
Figure2toFigure4.
fertilizer. The effective amount of applied N (10 g N adilutesolutionandasprayersystem,whichallowed
tree−1) by 15N-enriched ammonium sulfate was de- to spray each quadrant several times and thus ensure
ducted from the routinely applied N fertilizer. The ahomogeneousapplication.Thelitterlayerwascare-
nutrients were added uniformly on the surface of the fully removed before the application and distributed
mineral soil in a square of 4 m2 around each stem. evenly afterwards.
The tracer was applied to 1 m2 areas at a time using
216
uPlant and soil sampling 15N (cid:2)mgtree(cid:1)1(cid:3)(cid:4)(cid:1)(cid:5)biomass
biomass leaf,branch,stem
(cid:2)kgtree(cid:1)1(cid:3)(cid:6)15N (cid:2)mgkg(cid:1)1(cid:3)(cid:7)
leaf,branch,stem
The N isotope composition was measured in the four
tree species before the tracer application in October Recovery of 15N in tree and soil was determined in
1998,twoweeksafterthetracerapplicationon25–27 two different ways, as the ratio of uptake to applica-
January, and on 18/19 February, 23 March, 15–23 tion for the entire cropping system as shown in Fig-
April, 1 July and 8/9 November 1999. In February, ure1(NitrogenSystemRecoveryNSR)andforsingle
March and July, only leaf samples were collected, tree species (Nitrogen Tree Recovery NTR):
whereas at the other dates also stem and branches
15N (cid:2)mgtree(cid:1)1(cid:3)
were sampled.At least 10 leaves from random loca- NSR(cid:2)%(cid:3)(cid:4) biomass (cid:6)100
tions on each tree were collected including old and 15N (cid:2)mgsystem(cid:1)1(cid:3)
fertilized
young leaves exposed to sun or in the shade. Stem
samples were obtained with a drill (8 mm diameter) 15N (cid:2)mgtree(cid:1)1(cid:3)
NTR(cid:2)%(cid:3)(cid:4) biomass (cid:6)100
along the trunk to its center, branches were cut and 15N (cid:2)mgtree(cid:1)1(cid:3)
fertilized
pieces were randomly collected from young and old
parts (at least 10 samples per tree).
Totalapplication(100%)was9mg 15Nexcesstothe
InDecember1998andJanuary1999,soilsamples
system as shown in Figure 1, and 1, 1, 3, and 4 mg
were obtained from 0–0.1, 0.1–0.3, 0.3–0.5, 0.5–0.8,
15Nexcess to single tree species of cupuassu, Brazil
0.8–1.2, 1.2–2 m, inApril and November 1999 addi-
nut, annatto and peach palm. Recovery of 15N in be-
tionally at 2–3, 3–4, 4–5 m depths. Four subsamples
low-groundbiomasswasnotdetermined.Itmaycon-
were taken from each depth at 0.5–0.8 m distance
stitute a large part of total plant recovery, more for
from the trunk under those trees which received 15N,
peach palm (root-to-shoot ratio 1.0 for heart of palm
and combined to one sample per replicate.
production)thanforBrazilnut,cupuassuandannatto
(root-to-shoot ratio 0.3–0.4; Haag (1997)).
Determination of biomass and calculation of 15N
uptake
Nitrogen isotope analyses
In September 1998, April and December 1999, total
The leaf samples were dried at 70 °C for 48 hours.
above-ground biomass was determined using allom-
The soil samples were air-dried at room temperature
etricrelationshipsinordertocalculatetotalNuptake
and all samples were finely ground with a ball mill.
and 15Nrecovery:cupuassu(woodybiomass=18.59
The 15N-enriched samples were analyzed using an
× dia 2.82, N = 7; leaves = 4.07 × dia
stem at 0.2m stem at ElementalAnalyzer(CarloErbaNA1500;forDumas
3.42,N=36;allP<0.05forindependentsamples;
0.2m combustion)connectedtoanisotoperatiomassspec-
Wolf (1997)); Brazil nut (stem = 0.926 × f, N = 7;
trometer(FinniganMATdeltaE)viaasplitinterface.
branches=2.50×f1.51,N=7;leaves=10.36×f1.28,
Thenaturalabundanceof 15Ninplantandsoilbefore
N=79;wheref= (cid:1)(crosssectionarea
(at10,20,30%of application of the 15N-labeled fertilizer was deter-
) × height/10; all P < 0.05 for independent
total height) minedwithanelementalanalyzer(Fisons1108)cou-
samples; Wolf (1997)); annatto (stem + old branches
pled via a ConFlo II Interface to a delta S isotope
= 140.6 × dia 1.657, N = 4, P < 0.05, Wolf
stem at 0.2m ratio mass spectrometer (Finnigan MAT). Natural
(1997); young branches = 11.97 × dia + 7.02;
branch abundance of 15N was deducted from calculations of
leaves=24.87×dia +17.48,N=23;R2=0.71;
branch enrichedsamplestoestimatetherecoveryanduptake
own measurements); peach palm (total biomass =
distribution of the added 15N.
0.587×height–0.287,N=12;R2=0.93;ownmea-
surements). For production estimates of peach palm,
Statistical analyses
the trees that were cut during harvesting of the heart
ofpalmwerequantifiedseparatelyandtheNamounts
Statisticalanalyseswerecomputedbyanalysisofvar-
were added to the difference between values at the
iance (Statistica 5.0) using a randomized complete
beginning and the end of the experiment. Uptake of
blockdesignforcomparisonsbetweentreesindiffer-
applied 15N was calculated from the product of
ent plots and using a split plot design for compari-
above-ground biomass and 15N contents of leaves,
sons between trees in the same plot (Little and Hills
branches and stem, respectively:
217
Table1. Above-groundbiomassoffourdifferenttreecropsattheendoftheexperimentinDecember1999,biomassproductionduringone
yearasaproportionofthebiomassattheendoftheexperimentandNconcentrationsandtotalabove-groundNinamixedcroppingsystem
inthecentralAmazon.
Species Plantpart Above-groundbiomass Above-groundbiomass Biomassproduction Nconcentration Namount
[kgtree−1] [Mgha−1] [%yr−1] [gkg−1] [kgha−1]
Peachpalm totalplant 2.7d ±0.5 0.8d ±0.1 56.7b ±17.5 8.9 ±0.9 6.3d ±0.9
Brazilnut wood 169.7 ±15.2 15.8 ±1.4 60.6 ±6.7 6.4 ±0.4 101.3 ±11.8
leaves 63.1 ±5.2 5.9 ±0.5 64.4 ±7.3 23.1 ±0.7 137.8 ±13.0
totalplant 223.8a ±19.1 21.7a ±1.6 61.6ab ±6.9 nd 238.1a ±15.3
Annatto stem 9.3 ±0.2 1.4 ±0.0 8.6 ±1.4 6.3 ±0.5 9.3 ±0.8
branches 2.7 ±0.2 0.4 ±0.0 94.5 ±15.7 7.8 ±0.6 3.1 ±0.3
leaves 3.0 ±0.2 0.5 ±0.0 79.8 ±14.4 28.4 ±0.9 13.6 ±1.3
totalplant 15.3c ±0.4 2.4c ±0.1 86.4a ±15.0 nd 26.4c ±1.7
Cupuassu wood 19.4 ±1.4 1.8 ±0.1 52.2 ±6.7 5.3 ±0.4 10.6 ±1.6
leaves 18.6 ±1.6 1.7 ±0.2 66.7 ±9.0 20.0 ±0.5 35.9 ±3.7
totalplant 38.0b ±1.9 3.6b ±0.2 59.0b ±7.8 nd 46.5b ±3.8
Effect1 *** *** ** nd ***
1P<0.01(**),P<0.001(***).ValuesinonecolumnfollowedbythesameletterarenotsignificantlydifferentatP<0.05;meansand
standarderrors(n=12).ndnotdetermined.
1978). For the analysis of the foliar (cid:2)15N values, the Enrichment of 15N in plant and soil
logarithmic values were used due to inhomogeneity
of variances. In case of significant effects, individual Theuptakeofapplied 15Nwasrapidandalltreespe-
cell means for the respective level were compared cies had the highest foliar 15N enrichment during the
usingleastsignificantdifferences(LSDatP<0.05if period14to96daysafterfertilization(Figure2).The
not indicated otherwise) (Little and Hills 1978). enrichmentinbothpeachpalmandannattodecreased
rapidlyafterwardsbutremainedrelativelyconstantin
cupuassu. The highest relative enrichment was noted
Results in peach palm. Cupuassu, peach palm, and annatto
had a higher 15N enrichment when the fertilizer was
Biomass and N accumulation appliedunderneaththeirowncanopy,whereastheen-
richment did not differ according to the place of ap-
Thehighestabove-groundbiomasswasfoundinboth plication for Brazil nut. Only 18–43% of its foliar N
wood and leaves of individual Brazil nut trees, the derived from the fertilizer N which Brazil nut re-
lowest in peach palm (Table 1). On an area basis ceiveddirectlybyaplacementarounditsstem,while
peachpalmstillshowedthelowestbiomass,although 8–12% came from the fertilizer N applied to cu-
four peach palm trees were planted for every Brazil puassu, 12–28% and 23–54% from that applied to
nut or cupuassu. Annatto branch biomass had the annattoandpeachpalm,respectively(rangeindicates
highest relative production during the experimental variability over time; Figure 3). In contrast, the other
periodwithanincreaseofmorethan90%inoneyear tree species took up more than 85% of the fertilizer
(Table 1). Foliar N contents were highest in annatto Nfromthefertilizedareaunderneaththeirowncano-
(28.4gkg−1),whereastotalabove-groundNaccumu- pies. Whereas the proportion of uptake from the N
lation was largest for Brazil nut (238 kg ha−1), fol- directly applied around the stem of the trees de-
lowedbycupuassu(47kgha−1),annatto(26kgha−1) creased with time for peach palm, annatto and cu-
and peach palm (6 kg ha−1) (Table 1). puassu, it increased for Brazil nut (Figure 3). Conse-
quently, the total uptake of 15N by Brazil nut from
the area underneath its own canopy increased during
thestudyperiod(Figure4).Bytheendoftheexperi-
mentthe 15NuptakebyBrazilnutfromtheNapplied
218
Figure2. Foliar15Ndynamicsoffourdifferenttreecrops(A.toD.comparewithFigure1)asaffectedby 15Napplicationundertheirown
canopy or to the adjacent three tree crops (within each graph) from December 1998 (before the application of 15N enriched ammonium
sulfate)toNovember1999inamixedcroppingsysteminthecentralAmazon.Differencesandmaineffectscomputedbyanalysisofvari-
ance;nsnotsignificant,*,**,***significantatP<0.05,0.01,0.001,respectively;valueswiththesameletteracrossallspeciesatthesame
datearenotsignificantlydifferentatP<0.05(meansn=3).
around its stem (601 mg 15N tree−1) was in the order Recovery of applied 15N
of magnitude of the uptake from all other locations
and by all other trees in the system (869 mg 15N Attheendoftherainyseason54%oftheapplied 15N
tree−1)(Figure4).However,alsothetotal 15Nuptake were recovered in plant and soil (Table 2). Less 15N
byBrazilnutfromfertilizerappliedtotheothertrees was taken up by plants (25%) than was found in the
was significant: Brazil nut took up more N from the soiltoadepthof5m(29%).Therecoveryinthesoil
fertilizer applied to annatto (only by the end of the decreased from 73 to 29 to 7% throughout the year
experimental period) or peach palm than these tree whereas it increased in the plants from 14% in Janu-
species themselves (Figure 4). ary to 25% inApril but decreased to 17% in Decem-
ber. During the same time the total recovery in plant
219
Figure3. SpatialdistributionofrelativefertilizerNuptakebyfourdifferenttreecrops(A.toD.comparewithFigure1)fromNapplied
undertheirowncanopyortotheadjacentthreetreecrops(withineachgraph)inamixedcroppingsysteminthecentralAmazon.Values
abovecolumnsshowthesumoftheatom%15Nexcess;maineffectscomputedbyanalysisofvariance;nsnotsignificant,*,**,***signif-
icantatP<0.05,0.01,0.001,respectively(meansn=3).
and soil decreased from 87 to 54 to only 24% (data erywasnotsignificantlydifferentbetweenanyofthe
not shown). trees. In the above-ground biomass, the largest
In relation to the amount applied to each tree (ni- amount of 15N applied directly to the tree was ini-
trogen tree recovery NTR, equation 3), soils under tially recovered in Brazil nut and cupuassu, the low-
cupuassu tended to have slightly lower 15N recovery estinpeachpalm(P<0.05).After10months,Brazil
than soils under Brazil nut two weeks after applica- nut had taken more than half of the 15N applied to it
tion (P = 0.08; Figure 5).At other times, soil recov- (61%), followed by cupuassu (34%), whereas the
220
Figure4. Dynamicsof15Nuptakebyfourdifferenttreecrops(A.toD.comparewithFigure1)fromNappliedundertheirowncanopyor
totheadjacentthreetreecrops(withineachgraph)inamixedcroppingsystem(Figure1)inthecentralAmazonduringoneyear.Differences
andmaineffectscomputedbyanalysisofvariance;asterics(maineffects)andbars(LSD)indicatesignificantdifferencesbetweenlocations
ofapplicationforeachsamplingdate(differencesbetweenlineswithinonegraph):nsnotsignificant,*,**,***significantatP<0.05,0.01,
0.001,respectively;lettersindicatesignificantdifferencesacrossallsampledspecies(differencesbetweengraphsA.toD.)fortheeachsam-
plingdateatP<0.05(meansandstandarderrors;n=3).
lowest proportions of applied fertilizer were found in applied, but received only 11% directly around its
the above-ground biomass of annatto (11%) and stem.Thelowestefficiencywasnotedforpeachpalm,
peach palm (8%) (Figure 5). which retrieved 1.3% but received 45% of the total
Fromthewholecroppingsystem(nitrogensystem applied N to the entire system (system as shown in
recovery NSR, equation 2), the highest proportion of Figure 1).
the applied 15N after the rainy season was taken up The efficiency of investing N fertilizer was lowest
by Brazil nut with 12% and annatto with 8% (Ta- whenappliedtopeachpalm,asallplantstogetherre-
ble 2). Whereas most of the 15N taken up by either trieved only 5.9% of the total N applied to peach
annatto or peach palm originated from the N applied palm, although peach palm received 45% of the total
to the respective trees themselves, Brazil nut took up N in the system (calculating to 13% efficiency) (Ta-
4.6and3.4%ofthetotalappliedNinthesystemfrom ble 2). The highest efficiency was found for N fertil-
peach palm and annatto, respectively (Table 2). ized to cupuassu, from which 4.2% were taken up
Therefore, the high efficiency of Brazil nut was not while 11% were applied to cupuassu (38% efficien-
caused by uptake of the N fertilizer it received di- cy),withonlyslightlylowerefficienciesforNapplied
rectly(2.7%recovery),whichwaslowerthantheup- to annatto (33% efficiency) and Brazil nut (32% effi-
take by cupuassu from the N applied to cupuassu ciency).
(2.9%), but by an uptake of N applied to associated A large proportion of the unused N was found in
trees. Thus, Brazil nut recovered 12% of the total N thesoilunderpeachpalm(15%ofthetotalNapplied,
221
Table2. Systemrecovery(NSR,equation2)of15Nappliedtodifferenttreecropsasammoniumsulfatefertilizerinamixedcroppingsystem
inthecentralAmazonafter3monthsinApril1999.
15Nrecoveryby Recovery[%]of 15Nappliedto
Cupuassu Brazilnut Peachpalm Annatto totalarea
Cupuassu 2.9a ±0.4 0.5b ±0.4 0.1c ±0.0 0.1c ±0.0 3.6b ±0.4
A B B B
Brazilnut 1.0b ±0.6 2.7a ±0.6 4.6a ±2.0 3.4b ±2.0 11.7a ±3.0
C B A A
Peachpalm 0.0c ±0.0 0.0c ±0.0 1.2b ±0.2 na 1.3b ±0.2
B B A
Annatto 0.2c ±0.1 0.3b ±0.1 na 7.4a ±2.4 7.9a ±2.4
B B A
Sumofplants 4.2 ±0.4 3.5 ±0.5 5.9 ±1.7 10.9 ±4.4 24.5 ±4.2
B B B A
Soil(0–5m) 3.1 ±0.4 3.0 ±0.9 14.9 ±1.9 8.3 ±2.0 29.3 ±0.7
C C A B
Totalsum 7.3 ±0.3 6.5 ±0.3 20.8 ±2.1 19.2 ±3.0 53.8 ±6.0
B B A A
Applied 15N[g] 1(11) 1(11) 4(45) 3(33) 9(100)
andtreesperex-
perimentalunit([%
oftotal])according
toFigure1
na=notapplicable:rowsofannattoandpeachpalmarenotadjacent.Valuesinonecolumnorrowfollowedbythesamesmallorcapital
letter,respectively,arenotsignificantlydifferentatP<0.05;meansandstandarderrors(n=3).
being 33% of the amount it received directly). Sub- was practiced in the cited study. Therefore, our val-
stantially less N remained in the soil under annatto uesfortotalNuptakearetypicalforagroforestswith
(8.3% of the total N applied, being 25% of the similar species composition.
amount it received). Biomass and N uptake by roots were not assessed
inthepresentstudyandtotalNsequestrationinplant
biomasswasthereforeunderestimated.Usingamaxi-
Discussion mum estimate for root-shoot ratios (Haag 1997) and
root N contents total recovery may only slightly in-
Biomass and nitrogen uptake creasefrom53to62%.Thiscalculationassumessim-
ilarNconcentrationsinrootsasinabove-groundbio-
Above-ground biomass of all trees determined in our mass which is most likely much smaller as
study was similar to that determined in an extensive demonstrated by McGrath et al. (2000). The conclu-
study including destructive sampling of entire trees sions about the distribution of N uptake are not af-
conducted by Schroth et al. (2002) in the same ex- fected by neglecting root N contents, since the an-
periment. Nitrogen contents of leaf and woody bio- natto,Brazilnutandcupuassuhavesimilarroot-shoot
mass were slightly higher than those from 6- to ratios(Haag1997)andpeachpalmhasverylowtotal
8-year-old Brazil nut, peach palm and cupuassu (not biomass.
available for annatto) reported by McGrath et al.
(2000) from the southernAmazon basin.This can be
explained with the fact that no annual fertilization
222
2000). The restricted lateral root activity of pruned
peachpalmwasassumedtoberesponsibleforthelow
utilization of biologically fixed N from an inter-
cropped legume cover (Lehmann et al. 2000). Addi-
tionally, pruning the peach palm for heart of palm
harvest also decreased root activity in the subsoil at
the same site (Lehmann et al. 2001b).
The high proportion of N uptake by Brazil nut
from associated trees may not only be a result of an
uptake of N at the topsoil, but may also be derived
from subsoil N. Already two weeks after N applica-
tion, significant amounts were found at 0.8 to 2 m
depth and up to 5 m depth three months later (Din-
kelmeyer2000).Wewerenotabletoidentifywithour
experimental approach whether the trees were taking
up fertilizer N from the topsoil or the subsoil. The
strongtaprootformedbyBrazilnut(Haag1997)may
indicateasignificantuptakealsofromthesubsoil,al-
though Lehmann et al. (2001b) could not verify a
pronounced subsoil root activity. However, since the
total uptake by Brazil nut as shown in the present
studyisveryhighevenalowrelativeuptakefromthe
subsoil may still result in a relevant amount of sub-
soil N depletion.
Nitrogen use effıciency and nitrogen losses
Two mechanisms contribute to high fertilizer N up-
takebyamixedtreecroppingsystem:(1)highNup-
Figure 5. Recovery of the 15N applied to each tree (single-tree
observation;NTRfromequation3)initsownabove-groundbio- takefromthefertilizerdirectlyappliedtothetree,and
mass (I.) and in the soil (II.) in a mixed cropping system in the (2) high nutrient uptake by associated tree crops. For
centralAmazonduringoneyear.Differencesandmaineffectscom- example, the efficiency of the N applied to cupuassu
puted by analysis of variance; asterics (main effects) and bars
and annatto was not only an effect of a high uptake
(LSD)indicatesignificantdifferencesbetweentreesforeachsam-
by cupuassu or annatto, respectively, but a co-uptake
pling date: ns not significant, *, **, *** significant at P < 0.05,
0.01,0.001,respectively;LSDbarsarenotshownifmaineffects byBrazilnut.TheefficiencyoftheNappliedtoBra-
werenotsignificant;lettersindicatesignificantdifferencesbetween zil nut was lower than that to cupuassu and annatto
samplingdatesforthesamespeciesatP<0.05(meansandstan- due to the fact that no other tree took up N from the
darderrors;n=3).
fertilizer applied to Brazil nut. The larger uptake of
N by Brazil nut as compared to the amount that the
Uptake distribution of applied N fertilizer
treeactuallyreceivedbyfertilizerapplicationdemon-
stratestheimportanceofintroducingtreespecieswith
Brazil nut had the most widespread root activity
extensive root activities into plantations of trees that
amongthestudiedtreecrops,takingupmoreapplied
have spatially restricted root activities.
N from neighboring trees than from the fertilizer ap-
ThehighefficiencyoffertilizerNusebyBrazilnut
pliedunderitsowncanopy.Brazilnutwasthetallest
may be due to a possible uptake from the subsoil as
treewiththelargestabove-groundbiomassandNac-
discussed above. Both an uptake from the topsoil but
cumulation in the studied cropping system. This will
especiallyfromthesubsoilwillresultinlowerleach-
certainlyreflecttheamountofbelow-groundbiomass.
ing losses, which are generally large in the studied
Peach palm and annatto were periodically pruned
soil due to high rainfall (Rozanski et al. 1991). The
whichusuallydecreasesrootgrowthandextensionas
soils in the central Amazon are strongly weathered
shown for an acacia in Kenya (Peter and Lehmann
and have high anion exchange capacity due to varia-