SE

GLU

a

ARRA

KMPInC

1

csistItib

tdt

0d

Environmental and Experimental Botany 64 (2008) 180–188

Contents lists available at ScienceDirect

Environmental and Experimental Botany

journa l homepage: www.e lsev ier .com/ locate /envexpbot

hoot and root competition in potato/maize intercropping:ffects on growth and yield

ustave Nachigera Mushagalusa, Jean-Francois Ledent, Xavier Draye ∗

aboratoire d’ecophysiologie et d’amelioration vegetale, Faculte d’Ingenierie biologique, agronomique et environnementale,niversite catholique de Louvain, Place croix du Sud 2-11, 1348 Louvain-la-Neuve, Belgium

r t i c l e i n f o

rticle history:eceived 23 August 2007eceived in revised form 13 May 2008ccepted 20 May 2008

eywords:aize

otatotercropping

ompetition

a b s t r a c t

Interspecific competitive relationships and their effect on yield have been analysed in the associationof potato and maize, two species with contrasting patterns of root and shoot systems establishment.Greenhouse experiments were carried out under three configurations (NC: no interspecific competition;FC: shoot and root interspecific competition; SC: shoot-only interspecific competition). Despite largevariations between replicate experiments associated with seasonal effects, the study revealed consistentpatterns of competition for above- and below-ground resources. Light interception in FC and SC wasdominated by potato (60%) during the first 45 days after planting and by maize thereafter (80%). The extrashade caused by the companion crop increased soil moisture by up to 10% in SC treatments. The yieldof the two species responded in opposite ways to SC, which was consistent with asymmetric patternsof competition between the two species. In potato, FC reduced tuber yield (number and size) by 4–26%,while SC increased tuber size (compared to NC) by 3–39%. In maize, FC reduced LAI and plant heightby up to 45%, shoot and root dry mass, nutrient content, yield, the weight of 100 grains and harvestindex by ca. 30–100%, while SC affected all but LAI and plant height. It appears that the contrast betweenthe progressive installation of the maize root system and the rapid early extension of the potato root

system is amplified by the restriction of maize root development under competition, which leads to closeinterdependencies between root and shoot competitive relationships. Although the specific effects ofroot competition cannot be uncovered by this set of experiments, competition effects on maize in the

g see

tpM(am

rppae

potato/maize intercroppin

. Introduction

Intercropping, i.e. the simultaneous cultivation of two or morerops in the same field is practised in many regions of the world. Ineveral scenarios of species, region and climate, intercropping canncrease total yield per land area compared to the sole crop of theame crops. This effect is commonly attributed to the complemen-arity of resource capture patterns by crops (Rodrigo et al., 2001).ntercropping is also used for soil erosion management, pest con-rol and soil fertility improvement, but is most widely practicedn countries where arable land is scarce, where it contributes toiodiversity and food security.

Among a number of species combinations that are found inropical areas, the intercropping of maize and legumes is widelyocumented, which can be explained by the complementarity ofhe two crops in mineral nutrition and by their world-wide impor-

∗ Corresponding author. Tel.: +32 10 472092; fax: +32 10 472021.E-mail address: xavier.draye@uclouvain.be (X. Draye).

obLwidi1

098-8472/$ – see front matter © 2008 Elsevier B.V. All rights reserved.oi:10.1016/j.envexpbot.2008.05.008

m to primarily related to light availability in the mixed canopy.© 2008 Elsevier B.V. All rights reserved.

ance. This paper focuses on the potato/maize association, which isractised in Latin America (Midmore et al., 1988), Asia (Liu andidmore, 1990; Vander zaag and Demagante, 1990) and Africa

Ifekwe et al., 1989; Bouwe et al., 2000; Ebwongu et al., 2001). Thisssociation takes advantage of the complementary food values andorphologies of the two species.The optimization of cultivation practices under given envi-

onmental conditions requires a thorough understanding of theatterns of resource capture by individual plants and how theseatterns depend on morphology. These points require specialttention in intercropping systems combining species with inher-ntly different morphologies, where asymmetric distributionf capture organs is likely to induce dominance relationshipsetween plants which may affect their performance (Ozier-afontaine et al., 1999). It is worth noting that the presence of

eeds in a crop raises very similar problems. Given these close

nterspecific interactions, the outcome of intercropping largelyepends on available resources and on every condition influenc-

ng the phenology and growth of each species (Casper et al.,998).

and E

awmg1fimadbc

rtdaBatp

emtppoteW

c(Mymottea

2

2

cae(ttrPIcacsm

w

1dt1tRfon((3lsssdTs

iabpa(wtiwctev

vEmorning to restore field capacity. This interval was short enoughto preclude the occurrence of severe water deficit and long enoughto allow the reliable quantification by TRD probes of the decreaseof soil water content (see below). Protection against aphids andwhitefly was insured with sticky yellow traps placed above each

G.N. Mushagalusa et al. / Environmental

In the potato/maize association, competition for light might ben issue as the leaves of potato and maize exploit different strataithin the canopy. Maize, for example, has rather high require-ents for light and responds negatively to shade, which reduces

rowth and delays the appearance of leaves and roots (Pellerin,991). However, because potato height seldom exceeds 1 m in theeld against up to 3 m for maize (depending on variety and environ-ent), the latter is commonly regarded as the dominant plant in the

ssociation when the two species are planted simultaneously. Evi-ently, the dynamics of development in time and space should alsoe considered as it may strongly depend on variety and cultivationonditions (Midmore et al., 1988; Ebwongu et al., 2001).

There are less data on the importance of competition for soilesources in the potato/maize association. The two species differ byheir root system development in time and space. Potato root lengthensity is generally about one third of that produced by cereal crops,nd is generally higher in the top soil (Gregory and Simonds, 1992).ased on these contrasting soil exploration patterns, it is gener-lly believed that the combination of the two species may improvehe efficiency of soil water and nutrient uptake throughout the soilrofile.

There are, however, a number of reports on the detrimentalffects of interspecific competition for soil resources in other cropixtures. Root competition during the early season has been found

o decrease the initial growth and reduce the ability of individuallants to compete for light (Cahill, 1999; Aerts et al., 1991). Not sur-risingly, several studies also indicate that the relative importancef root and shoot competition between species can change duringhe season according to the development of the partners (Belchert al., 1995; Cahill, 2002; Casper et al., 1998; Carlen et al., 2002;ilson, 1988; Wilson and Tilman, 1995).Potato/maize intercropping has been mostly discussed under

onditions of high temperatures in Latin America and AsiaMidmore, 1990; Vander zaag and Demagante, 1990; Liu and

idmore, 1990), with a focus on the improvement of the potatoield by shade cast by maize. In the present study, the effect ofutual shade between potato and maize in the presence or absence

f root competition is analyzed. The objectives of this study wereo investigate the relative importance of shoot and root competi-ion between maize and potato in mixture, estimated through theirffect on yield and morphological parameters (height, leaf area, rootnd leaf dry mass).

. Material and methods

.1. Description of experiments

Three replicated greenhouse experiments (2002, 2003a,b) werearried out in Louvain-la-Neuve, Belgium. The varieties Desireend Tripoli were used, respectively, for potato and maize. Eachxperiment followed a complete random blocks design with two2003a, 2003b) or three (2002) blocks and three treatments. Thehree treatments comprised sole crops (no interspecific compe-ition, labelled MNC and PNC for maize and potato samplings,espectively), full interspecific competition treatments (MFC andFC) and shoot interspecific competition treatments (MSC and PSC).ntraspecific competition was involved in all treatments and wasonsidered as part of the common environment. Possible inter-ctions between intra- and interspecific competitions were thus

onfounded with the effect of treatments, but we assumed thatuch interaction effects were small compared to the effect of treat-ents.Plants assigned for sampling were grown in rectangular ply-

ood frames (open on top and bottom, Length × Width × Height:

Fas

xperimental Botany 64 (2008) 180–188 181

.2 m × 0.15 m × 0.60 m) standing above ground on a pit (sameimensions) sheathed with a plastic film to insure isolation fromhe surrounding soil (Fig. 1). Each box/pit element (L × W × H:.2 m × 0.15 m × 1.20 m) contained 108 L of a 2:3 volumetric mix-ure of universal compost (peat and bark, fertilized and limed):hine sand (0–2 mm) which facilitates the separation of roots

rom the soil at the time of excavation. The chemical analysisf the compost (before sowing) gave the following results: totalitrogen (0.35%, Kjeldhal), P2O5 (0.06%, ICP-AES), K2O (1.0%), MgO0.26%), CaO (0.63%), Fe2O3 (0.62%), Na2O (0.30%), Al2O3 (2.14%), Zn13.5 mg/kg). This provided a total amount of 15.8 g N, 1.2 g P and7.2 g K per box, containing up to 5 plants in the FC treatments. Aarge drainage pipe laid down horizontally at the bottom of the pitecured the hydraulic isolation of each box-pit unit from the sub-oil, allowing a finer control of water availability in the accessibleoil. All root observations were performed in the box volume. Bor-er plants were grown in pots (L × W × H: 0.4 m × 0.4 m × 0.3 m).hey were lifted up or down during the experiment to maintainimilar plant heights for box and border plants.

The arrangement of plants in the three treatments is illustratedn Fig. 2. In each maize or potato treatment, eight plants wererranged as two planting rows, with 50 cm between plants andetween rows. Measurements were performed on the four centrallants, grown in two boxes. This arrangement should insure thatll treatments shared the same level of intraspecific competitionfour plants in two boxes). Interspecific competition (SC and FC)as created by adding six plants of the competing species around

he four central plants. Such additive design corresponds to the wayntercropping is implemented in tropical areas. A traditional design

ould have counted on two additional rows of border plants butould not be applied here for practical reasons. However, due tohe consistent arrangement of sampled and border plants, borderffects were systematic and should not have introduced additionalariability.

Solar radiation was supplemented all day long with artificial Hgapour lamps yielding 150 �mol/m2/s PAR at the top of the canopy.very 2 days from sowing to harvest, water was applied early in the

ig. 1. Schematic representation of the substrate containers. (A) Plywood box (opent the top and the bottom). (B) Plastic-sheathed pit. (C) Drainage pipe. (D) Groundurface of the greenhouse.

182 G.N. Mushagalusa et al. / Environmental and Experimental Botany 64 (2008) 180–188

Table 1General information on the three experiments

2002 2003a 2003b

Date of planting 11 February 09 January 02 MayDate of harvest 18 May 09 April 04 AugustAverage day temperature (◦C) 20–30 20–32 25–40Average night temperature (◦C) 9–18 15–18 18–20PAR at the top of the canopy (�mol m−2 s−1)a 400/500 350/450 500/880Fertilization b – –Relative humidity (%) 25–50 25–45 35–60

perimwith 2

0 nd 9.9

bT

2

h

Fpsa

pb

a Minimum and maximum PAR values (including artificial lighting) during the exb In 2002 only, each box was supplied twice, before and during tubers initiation,

.91 NaH2PO4·2H2O and (in mg l−1) 248 H3BO3, 11.7 ZnSO4·7H2O, 79 MnCl2·4H2O a

ox. Other general information about these experiments is listed inable 1.

.2. Measurements during the experiment

Plant height was monitored weekly between emergence andarvest on the four plants dedicated for sampling (Fig. 2). The

ig. 2. Schematic representation of the experimental design (one block). Potatolants are represented by open symbols and maize plants by closed symbols. Thequare symbols indicate the plants dedicated for sampling. The two planting rowsre represented as dotted lines (oriented N–S) and the boxes as grey rectangles.

fmmm(leta

w2eui2tsimi

acttcam(btcie

2

iwwawao7fH

ent between 11:30 and 12:30.l of a solution containing (in g l−1) 4.72 Ca(NO3)2·4H2O, 0.87 K2SO4, 1.46 FeEDTA,

8 CuSO4·5H2O.

henological development of maize was estimated as describedy Ledent and Mouraux (1990). The leaf lamina was consideredully expanded when the ligule was visible. The total leaf area of

aize was calculated by summing individual leaf areas (ILA) esti-ated from non-destructive measurements of leaf length (LL) andaximum leaf width (LW) and using the equation ILA = K × LL × LW

K = 0.75) (Girardin, 2000). The same formula was applied to potatoeaf area, using a value of K = 0.55 calibrated from 10 leaves of differ-nt ages in proportions estimated on eight plants. Plant height wasaken at the ligule of the last leaf lamina fully unfolded for maizend at the top of the canopy for potato.

During experiments 2003a and 2003b, one box in each blockas equipped with six time domain reflectometry (TDR) probes,0 cm long, placed horizontally at 20, 40 and 60 cm depth underach of the two sampled plants. Soil water content was estimatedsing a Tektronix impulse generator and a conversion formula cal-

brated with high organic content substrate (Souza and Matsura,003). Measurements of soil water content were taken early inhe morning before each watering (every 2 days—all boxes beingupplied to field capacity) and 6 h after watering, thereby reflect-ng the water uptake activity of the plants. Soil temperature was

easured at 10–11 and 15–16 h with thermocouple sensors (Hannanstruments) located at 15 cm depth under each plant in the boxes.

During experiments 2003a and 2003b, the photosyntheticallyctive radiation (PAR) was measured at several heights in theanopy using a sunfleck ceptometer (Delta-T Devices Ltd). In thereatments involving interspecific shoot competition (FC and SC),he PAR was measured (1) at the top of the dominating species in theanopy, (2) at the top of the dominated species in the canopy and (3)t the soil surface. A light extinction coefficient was calculated fromeasures (1) and (2) for the dominating species and from measures

2) and (3) within the mixed canopy. Fractional light interceptiony each species was derived according to Wallace (1995). In the NCreatment, two measurements were carried out, at the top of theanopy and at the soil surface. All measurements were made dur-ng clear days between 11:30 and 12:30. Measurements were takenvery 10 days from 25 to 85 days after sowing.

.3. Measurements at harvest

Plants dedicated to sampling were harvested 90 days after plant-ng. The boxes were opened and the substrate was washed away

ith a gentle flow of water. For potato, shoot and tuber fresheights were measured, along with the total number of tubers

nd the diameter of each tuber. Root, tuber, leaf and stem dryeight were measured, including dead material, after desiccation

t 80 ◦C for 72 h. Tuber dry mass content (TDMC) was measuredn 250 g samples of tubers which were sliced and oven dried for2 h, and tuber dry weight (TDW) was calculated as total tuberresh weight × TDMC. Finally, the harvest index was calculated asI (%) = (TDW/total dry biomass) × 100.

and E

aapy

Iettp

ttm(peb

Epct(toaattJdo

G.N. Mushagalusa et al. / Environmental

For maize, aerial parts and the total root system were oven-driedt 80 ◦C for 72 h and weighed. Ears of every plant were oven-driedt 80 ◦C for 72 h, shelled and weighed to obtain the grain yield perlant. The weight of 100 grains and harvest index (HI (%) = (grainield/total dry biomass) × 100) were also determined.

The nutrient concentration in the maize shoot was analyzed byCP-AES to estimate the effect of interspecific competition on min-ral nutrition of maize. Nitrogen content could not be measured dueo accidental loss of samples during analysis. The nutrients concen-ration in potato is not reported because the vegetative growth ofotato was not affected by interspecific competition with maize.

Relative reductions in plant growth due to interspecific compe-ition were calculated according to Gibson et al. (1999) assuminghat the monospecific competition was similar in all treat-

ents (see above). The effect of interspecific full competition

EFC) was estimated by comparing the dry weight (Y) of FClants to that of NC plants: EFC = ((YFC − YNC)/YNC) × 100. Theffect of interspecific shoot competition (ESC) was determinedy comparing the dry weight of SC plants to that of NC plants:

2

o

Fig. 3. Progression of leaf area index (LAI) during the season. PNC (�), MNC (�),

xperimental Botany 64 (2008) 180–188 183

SC = ((YSC − YNC)/YNC) × 100. The effect of interspecific root com-etition could not be directly estimated due to the lack of a pure rootompetition treatment. However, a combined effect of root compe-ition and of the interaction between root and shoot competitionERC) was calculated by subtracting the mean of SC plants fromhat of the FC plants: ERC = ((YFC − YSC)/YNC) × 100. In the absencef interaction between shoot and root competition, this term wouldpproximate the root competition effect. While some researcherscknowledge that interaction between the two forms of competi-ion is likely, they usually assume that its amplitude is limited inhe range of conditions encountered in experiments (Casper andackson, 1997). In addition, greenhouse (Wilson, 1988) and fieldata (Cahill, 1999) suggest that this latter assumption may be moreften valid than one would assume.

.4. Statistical analyses

Statistical inference on treatments at harvest was carriedut using a mixed model ANOVA according to the randomized

PSC (©), MSC (�), PFC (�), MFC (�); vertical bar: standard error on mean.

1 and Experimental Botany 64 (2008) 180–188

ctpmbfa

3

3

irm6tcBcihic(

3

tcmStnite

3

cp

e2er2ta(

ntamsonw

i

FM

Wt

84 G.N. Mushagalusa et al. / Environmental

omplete block design (Littell et al., 1996). There was impor-ant plant size variability among experiments. In 2003b thelants were larger, had more leaves and accumulated leaf areauch more so than in 2003a and 2002. As the interaction

etween experiment and treatment was statistically significantor many parameters, the three experiments were analyzed sep-rately.

. Results

.1. Light interception

During the first month of the experiment, potato exhib-ted a rapid increase in LAI (Fig. 3) and plant height (Fig. 4)esulting in a dense coverage of the soil surface in all treat-ents. Potato plants were taller than maize and intercepted

0% of the incident radiation reaching the top of the canopy,o the detriment of maize interception, which was signifi-antly affected in comparison with the NC treatment (P < 0.02).etween 35 and 45 days after planting, the fractional light inter-eption of potato progressively decreased, indicating a changen dominance relationships as maize plants were growing ineight. After 45 days, maize was taller than potato (Fig. 4) and

ntercepted up to 80% of the incident radiation. These light inter-eption patterns were remarkably consistent among experimentsFig. 5).

.2. Soil moisture

In potato as well as maize treatments, shading due to the addi-ion of the companion crop (SC relative to NC) increased soil waterontent (Fig. 6). This effect was observed early in the maize SC treat-ent, when maize was in the shade of potato, and later in the potato

C treatment, when potato was in the shade of maize. No increase ofhe soil water content was detected in the FC treatment, which mayot be surprising as the companion crop was also taking up water

n the same box, but could alternatively be due to some interac-ion (i.e. non-additive effects) between root and shoot competitionffects.

.3. Potato development and yield

The response of potato to the different treatments was ratheronsistent among experiments despite important differences oflant growth between experiments (Table 2).

The tuber yield under NC conditions approached high field lev-ls. Compared to NC, FC reduced the tuber yield (significant in003a and 2003b) by 4.1–26.8%. This effect, which was also appar-nt in the dry weight of tubers (significant in 2003a and 2003b),esulted from a reduction of the number of tubers (significant in002 and 2003b) and, in 2002, from a shift of tuber size distribu-ion towards smaller sizes. FC did not significantly affect the shootnd root dry weight, the root/shoot allocation, the harvest indexnot significant in 2002 and 2003a) and the LAI.

Compared to NC, SC increased tuber yield by 2.4–28.5% (sig-ificant in 2002). This increase was the consequence of a shift ofuber distribution towards large sizes (best pronounced in 2002)nd could not be attributed to a change of TDW. Shoot dry weightay have benefited from SC (from 7 to 23.4%), but this effect was not

ignificant and was not paralleled with LAI differences. The effect

f SC on root dry weight was less consistent (−11.9 to +27.4%) andot significant. Neither the root/shoot ratio nor the harvest indexas consistently affected by SC.

Among experiments however, strong differences were observedn plant growth and in carbon allocation to shoot, roots and tubers.

lr(ta

ig. 4. Progression of plant height. PNC (�), MNC (�), PSC (©), MSC (�), PFC (�),FC (�); vertical bar: standard error on mean.

hile 2002 and 2003b results were close to expectations for potato,he 2003b experiment was remarkable with tuber yield and TDWess than one third those of the other experiments. The strongeduction of tuber size in 2003b was inversely proportional to LAI

Fig. 3) and root dry weight. High temperatures (35–40 ◦C) duringhe tuber development stage may have contributed to this strongllocation change.

G.N. Mushagalusa et al. / Environmental and Experimental Botany 64 (2008) 180–188 185

Table 2Yield and biomass of potato at harvest (90 days after planting)

TFW (g pl−1) TDW (g pl−1) Number of tubers (pl−1) SDW (g pl−1) RDW (g pl−1) RSR HI (%)

Diameter classes Total

<29 29–57 >57

2002PNC 922.3a 199.7a 3.3b 8.1a 2.6b 14.0a 101.1a 1.8ab 0.02a 66aPFC 884.8b 187.0a 4.4a 6.6ab 1.1b 11.7b 84.2b 1.5b 0.02a 68aPSC 1185.3a 182.6a 2.6c 4.6b 6.1a 13.2a 108.2a 2.2a 0.02a 62bS.E. 33.7 8.8 0.06 0.24 0.08 1.5 3.9 0.001 0.01 1.11CV (%) 11.7 16.1 6.3 12.7 8.5 38.9 14.0 24.5 6.5 8.2EFC (%) −4.1 −6.4 – – – – −16.7 −13.1 – –ESC (%) +28.5 −8.6 – – – – 7.1 27.4 – –ERC (%) −32.6 +0.02 – – – – −23.7 −40.6 – –

2003aPNC 720.3ab 150.0a 1.5a 6.0a 5.1a 12.6a 57.7a 1.4a 0.03a 71aPFC 680.5c 122.3b 1.5a 6.4a 5.1a 13.3a 66.4a 1.5a 0.03a 65aPSC 775.4a 158.5a 1.9a 6.6a 6.0b 14.5a 59.8a 1.5a 0.02b 69aS.E. 13.7 3.5 0.07 0.01 0.22 0.4 1.99 0.11 0.001 1.6CV (%) 5.4 6.8 11.4 4.9 11.3 9.2 9.16 22.3 13.5 11.0EFC (%) −5.52 −18.5 – – – – +15.2 +10.3 – –ESC (%) +10.4 +5.7 – – – – +3.7 +6.6 – –ERC (%) −13.2 −24.1 – – – – 11.5 +3.7 – –

2003bPNC 356.7ab 56.0a 6.4a 4.4b 1.9a 12.6b 251.2a 8.9a 0.04a 18aPFC 261.2c 40.5b 4.4b 2.8c 1.6a 9.0c 215.3a 6.5a 0.03a 14bPSC 364.6a 52.4a 7.6a 6.3a 2.3a 16.0a 309.8a 7.8a 0.03a 15bS.E. 9.0 1.2 0.6 0.07 0.07 0.4 10.6 0.17 0.002 0.24CV (%) 7.8 6.6 9.7 4.5 10.5 9.8 11.6 6.1 13.1 7.4EFC (%) −26.8 −27.7 – – – – −14.3 −26.6 – –ESC (%) +2.2 −6.3 – – – – +23.4 −11.9 – –ERC (%) −29 −21.4 – – – – −37.6 −14.6 – –

TFW: tuber fresh weight; TDW: tuber dry weight; RDW: final root dry weight; SDW: final shoot dry weight; RSR: root shoot ratio; HI: harvest index; PNC: no interspecificcompetition; PFC: full interspecific competition; PSC: shoot interspecific competition. Exx: effect of full, shoot or root competition. Within a given experiment, numbersfollowed by the same letter (in a column) are not significantly different (P < 0.05).

Table 3Yield and biomass of maize at harvest (90 days after planting)

SDW (g pl−1) RDW (g pl−1) RSR (g pl−1) Yield W100 HI (%)

2002MNC 66.0a 4.3a 0.06b 45.4a 18.4a 64.6aMFC 35.2c 2.8c 0.08a 12.4c 10.5c 32.6bMSC 53.5b 3.7b 0.07b 33.2b 14.2b 58.0aS.E. 0.78 0.11 0.003 0.9 0.25 1.3CV (%) 7.4 15.2 24 14.5 8.6 12.1EFC (%) −46.6 −35.3 – −72.7 −42.9 –ESC (%) −18.8 −12.1 – −26.9 −22.8 –ERC (%) −27.8 −21.2 – −45.8 −20.1 –

2003aMNC 47.7a 3.7c 0.09a 35.6 15.2 69.2MFC 3.9c 0.07c 0.07b – – –MSC 17.2b 0.27b 0.10a – – –S.E. 1.01 0.06 0.007 – – –CV (%) 4.4 4.5 7.6 – – –EFC (%) −91.8 −98.2 – – – –ESC (%) −64 −92.6 – – – –ERC (%) −27.8 −5.6 – – – –

2003bMNC 167.1a 12.8a 0.079a 105.4a 19.8a 60.3aMFC 121.6b 7.1b 0.061a 51.7c 13.0c 38.7bMSC 186.7a 15.9a 0.087a 87.6b 16.4b 43.1bS.E. 6.0 0.8 0.006 3.1 0.85 2.13CV (%) 18.6 29.5 38.4 18.5 14.7 22.0EFC (%) −27.3 −44.7 – −51 −34.6 –ESC (%) +11.7 +23.8 – −17 −17.5 –ERC (%) −39 −68.5 – −34 −17.2 –

RDW: final root dry weight; SDW: final shoot dry weight; HI: harvest index; W100: weight of 100 grains; MNc: no interspecific competition; MFc: full interspecific competition;MSc: shoot interspecific competition; E: effect of full, shoot or root competition. Within a given experiment, numbers followed by the same letter (in a column) are notsignificantly different (P < 0.05).

186 G.N. Mushagalusa et al. / Environmental and Experimental Botany 64 (2008) 180–188

), PSC

3

mtrFdgraar

bwyhTr

tcwe

tttMtlaSrrwist

3

il

Fst

Fig. 5. Progression of the fraction of light interception. PNC (�), MNC (�

.4. Maize development and yield

The effects of interspecific competition on maize (Table 3) wereore pronounced than those on potato. It is clear from the NC data

hat maize growth was not optimal, which is to be linked with theelatively low PAR, especially in 2002 and 2003a. Compared to NC,C reduced significantly the shoot dry weight (−27 to −91%), rootry weight (−35 to −98%), yield (−51 to −100%) and weight of 100rains (−34 to −100%) in the three experiments. This treatment alsoeduced significantly LAI and plant height, which was most notice-ble in 2003a. The root/shoot ratio under FC was increased in 2002nd decreased in 2003a, while the harvest index was significantlyeduced in 2002 and 2003b and there was no yield at all in 2003a.

Relative to NC, SC also depressed plant biomass and yieldut in significantly smaller proportions than FC. The effect of SCas significant for SDW and RDW in 2002 and 2003a and for

ield and W100 in the three experiments. Neither LAI nor planteight seemed to be consistently affected by shoot competition.hese slight effects on plant growth occurred without change inoot/shoot allocation.

As for potato, strong differences were observed between thehree experiments. In 2003a, limiting irradiance at the top of theanopy negatively affected biomass production in all treatmentshile low early temperature (10–14 ◦C) caused a delay in maize

mergence of about 10 days (data not shown). While the combina-

teihw

ig. 6. Progression of soil moisture (cm3 cm−3) (×10−3) at 20 cm depth in experiments 20tandard error on mean. Because there is no difference between soil moisture at differenthis figure.

(©), MSC (�), PFC (�), MFC (�); vertical bar: standard error on mean.

ion of these effects depressed maize growth and yield in the NCreatment, ears were empty or contained no marketable grains inhe SC and FC treatments which exacerbated the shortage of light.

aize plants in these conditions may have been unable to achievehe minimum rate of root expansion required to allow a satisfactoryevel of nutrient uptake, especially for low-mobility nutrients suchs phosphorus for which deficiency symptoms were noticeable.uch dramatic effects did not occur in 2002, where maize expe-ienced less extreme light conditions, and was less dependent onoot system expansion given a point addition of fertilizers (Table 1)hich supplied readily available amounts of nutrients to the stand-

ng root system. This interpretation stresses the importance ofhoot/root interdependency, both above- and below-ground struc-ures acting as a sink for major resources captured by the other.

.5. Nutrient concentration in the maize shoot

The average nutrient concentration in the maize shoot at harvests outlined in Table 4 for some of the elements which exhibited theargest differences among years and treatments. Compared to NC,

he FC treatment consistently reduced the content of all reportedlements (significant in most cases). The effect of SC appeared to bentermediate between NC and FC. The nutrient content was globallyigher in 2003b than in 2003a for most elements. This coincidedith a larger root development in 2003b compared to 2003a (about

03a and 2003b. PNC (�), MNC (�), PSC (©), MSC (�), PFC (�), MFC (�); vertical bar:soil depth (20, 40 and 60 cm) only the soil moisture at 20 cm depth is presented in

G.N. Mushagalusa et al. / Environmental and E

Table 4Mean nutrient concentrations in the maize shoot (mg kg−1)

P K Mg Ca Fe

2003aMNC 4150a 23,620ab 1650.1a 3523a 87abMFC 2798b 21,596b 1086c 2134c 82bMSC 2798b 26,137a 1341b 2963b 96aS.E. 42.02 115.1 105.4 42.8 4.1

2003bMNC 3759a 23,274b 2061b 9506a 159abMFC 2641c 20,660c 2097b 6530b 146bMSC 2753b 25,616a 2372a 9503a 170aS.E. 25.6 122.8 55.6 65.4 13.1

Mis

tlifcm

4

ihrtarwdowiti

4

pbt(2(dpwtlacTdwp(ac

4(

tbcr

d1p1iraIctc

actbrmaa3tmstie

aiwtw

4

tnbwuPoanwgpb

not be relevant to validate this assumption. However, it provides

NC: no interspecific competition; MFC: full interspecific competition; MSC: shootnterspecific competition. Within a given experiment, numbers followed by theame letter (in a column) are not significantly different (P < 0.05).

hree times in terms of dry biomass) and a significant increase ofateral root length and density (data not shown), which resultedn a more than three times increase in root length and root sur-ace. This largely compensated for the reduced root:shoot ratio andontributed to an improvement of soil exploration and possibly ofineral uptake.

. Discussion

The growth of potato and maize in sole crop and in differentntercropping configurations has been recorded from planting untilarvest in order to investigate the relative importance of shoot andoot competition between the two crops and its evolution duringhe crop cycle. Despite the relatively small size of the experimentsnd the large variation observed between experiments, the studyevealed consistent patterns of light interception by the two speciesith a characteristic inversion of dominance relationships near 45ays after planting. The addition of a companion crop resulted inpposite responses of maize grain yield and potato tuber yieldhich were, respectively, decreased and increased under shoot

nterspecific competition. The study also reveals consistently thathe competition for soil resources is likely to play a significant rolen potato/maize intercropping.

.1. Evolution of light interception patterns during the crop cycle

Light interception in interspecific and monospecific stands isrobably the most illustrated aspect of competitive relationshipsetween neighbouring plants. In a number of crop combina-ions, as in the case of potato/maize (present study), shrub/grassTournebize and Sinoquet, 1995), sorghum/cowpea (Gilbert et al.,003), wheat/maize or wheat/soybean (Li et al., 2001), leek/celeryBaumann et al., 2001), leaf area distribution in the canopy haseterminant effects on light interception. A characteristic of theotato/maize association is the rather abrupt change which occurshen new maize leaves arise above the dense potato canopy. While

he young maize plant seems to be able to tolerate an episode ofow incident radiation when it is in the shade of potato (e.g. 2003b),slight delay of maize emergence due to unpredictable transient

onditions can have dramatic effect on the final yield (e.g. 2003a).he range of optimal sowing periods is also likely to be depen-ent on the environmental conditions and agricultural practiceshich may influence the duration of the periods during which one

artner is in the shade of the other and the strength of the shadeHall et al., 1992; Rajcan and Swanton, 2001). In this sense, thessociation’s yield might be more vulnerable than that of the solerops.

cpyS

xperimental Botany 64 (2008) 180–188 187

.2. Consequences of light interception patterns in intercroppingshoot competition)

One of the motivations of intercropping resides in the exploita-ion of the complementarity in the patterns of resource capturey the mixed crops (Rodrigo et al., 2001). In terms of solar energyapture, the potato/maize association relies on much more subtleelationships than a simple complementarity.

On the one side, the maize plant is clearly affected by low irra-iance (Fournier, 2000; Reed and Singletary, 1989; Schoper et al.,982; Setter et al., 2001) and, therefore, by the presence of a com-anion crop competing for light (Kropff et al., 1992; Braconnier,998; Cavero et al., 1999; Liedgens et al., 2004). As shown heren the case of early competition with potato, maize is not able toecover completely from the limited period of shade experiencedt young stages, and this has irreversible consequences on yield.n addition, this phenomenon is not limited to early stage of therop cycle (Setter et al., 2001). In a number of mixtures, maize ishus struggling more for light and suffering irreversibly from lightompetition than it is sharing light with the companion crop.

The potato plant, however, may also be affected by low irradi-nce. In a study by O’Brien et al. (1998) artificially shading the potatorop before or after the period of tuber initiation did not affecthe number of tubers, unless the incident radiation was reducedy more than 37%. Under continuous shade, TDW was ultimatelyeduced by as much as 40% (Sale, 1976). Intercropping conditionsay additionally affect temperature within the canopy and inducebeneficial microclimate for potato growth, especially when the

mbient temperature in the potato sole crop would be higher than0 ◦C (Midmore et al., 1988). Here, the presence of maize abovehe potato canopy affected soil temperature (data not shown) and

oisture and was beneficial for tuber fresh weight. In compari-on with the artificial shade data, these latter experiments suggesthat the indirect effects induced by maize during the period wheret dominates the canopy can at least compensate for the harmfulffect of low irradiance on potato.

The potato/maize association is therefore a clear example ofsymmetric relationships, where the ultimate outcome of lightnterception patterns would depend on a subtle balance between

hat can be afforded at the maize level (which strongly depends onhe relative development of the two crops) and the indirect benefithich can be expected at the potato level.

.3. Root competition patterns in intercropping

Potato and maize display very contrasting root system archi-ectures both in time and space. Potato may produce 90% of itsodal roots by the fourth leaf stage thanks to the abundant car-on resources in the planted tuber (Iwana et al., 1979; Iwana, 1998)hile the emergence of nodal roots in maize is progressive andsually synchronous with that of leaves (Demotes-Mainard andellerin, 1992; Girardin, 2000; Pellerin, 1991). In addition, the rootsf potato are produced at varied angles (from horizontal to vertical)nd are preferentially present in the top 30–60 cm of the soil (dataot shown) while those of maize display clear gravitropic responseshich allow them to reach lower layers. Based on these data, it is

enerally assumed that soil exploration by the two species is com-lementary and that the root system contribution to competitionetween maize and potato should be limited.

This study did not isolate the effects of root competition and may

onvincing evidence that the combination of root and shoot com-etition (compared to shoot competition alone) further reduces theield of maize and obviates the beneficial effect of shade on potato.oil water content data suggest that the effect on potato might be

1 and E

dwmstoseobtoap

tiaruis

remtt

A

(eAB

R

A

B

B

B

B

C

C

C

C

C

D

E

F

G

G

G

G

H

I

I

I

K

L

L

L

L

L

M

M

O

O

P

R

R

R

R

S

S

S

S

T

V

Wuse in intercrops and agroforestry. In: Sinoquet, H., Cruz, P. (Eds.), Ecophysiology

88 G.N. Mushagalusa et al. / Environmental

ue to the larger water uptake by the two species mixture, whichould suppress the beneficial cooling effect of the shade cast byaize, as a dry soil would be more prone to warming than a moist

oil. The case of maize is probably different because the detrimen-al effect of the early shade cast by potato also affects the growthf the maize root system and the capacity to rapidly colonize theoil. The latter effect would be especially important since potatostablishes most of it root system very quickly. The importancef fast exploration rate in the competition for soil resources haseen reviewed by Robinson (1996). When maize emerges abovehe potato leaves, the maize plant has therefore an underdevel-ped root system which is likely to hamper its competitive ability tocquire soil resources, which would contribute to the lower maizeerformance in FC compared to SC.

The interdependency between root and shoot was further illus-rated by the fact that fertilizer supply on maize in the SC treatmentn 2002 was able to promote maize growth, even though a sufficientmount of nutrient was present in the soil volume. Most likely,oot growth had been reduced by the competition for light and wasnable to counterbalance the progressive depletion of low mobil-

ty nutrients such as phosphorus in the vicinity of the standing rootystem.

Although the strict consequence of root competition cannot beevealed by this set of experiments, it appears that competitionffects on maize are primarily related to light availability in theixed canopy, but that they restrict root development and increase

he vulnerability of maize in front of the advanced development ofhe potato root system.

cknowledgements

The authors thank the Evangelisher Entwicklungstudienst-EEDGermany) for financial support to GM and two anonymous review-rs for constructive comments on the manuscript. XD is a Researchssociate from the Fonds de la Recherche Scientifique (FSR-FNRS,elgium).

eferences

erts, R., Boot, R.G.A., van der Aart, P.J.M., 1991. The relation between above- andbelow-ground biomass allocation patterns and competitive ability. Oecologia87, 551–559.

aumann, D.T., Bastiaans, L., Kropff, M.J., 2001. Competition and crop performancein a leek–celery intercropping system. Crop Science 41, 764–774.

elcher, J.W., Keddy, P.A., Twolan-Strutt, L., 1995. Root and shoot competition inten-sity along a soil depth gradient. Journal of Ecology 83, 673–682.

ouwe, N.B., Walangululu, M., Kidanemariam, H.M., 2000. Performance de 4 culti-vars de pomme de terre en culture associee avec le maıs et le haricot. In: AfricanAssociation Conference Proceeding, vol. 5, pp. 87–190.

raconnier, S., 1998. Maize–coconut intercropping: effect of shade and root compe-tition on maize growth and yield. Agronomie 18, 373–382.

ahill Jr., J.F., 1999. Fertilization effects on interactions between above- and below-ground competition in on old field. Ecology 80, 466–480.

ahill Jr., J.F., 2002. Interactions between root and shoot competition vary amongspecies. Oikos 99, 101–112.

arlen, C., Kolliker, R., Reidy, B., Lucher, A., Nosberger, J., 2002. Effect of season andcutting frequency on root and shoot competition between Festuca pratensis andDactylis gomerata. Grass and Forage Science 57, 247–254.

asper, B.B., Cahill Jr., J.F., Hyatt, L.A., 1998. Aboveground competition does notalter biomass allocated to roots in Abutilon theophrasti. New Phytologist 140,231–238.

avero, J., Zaragoza, C., Suso, M.L., Pardo, A., 1999. Competition between maizeand Datura stramonium in an irrigated field under semi-arid conditions. WeedResearch 39, 225–240.

emotes-Mainard, S., Pellerin, S., 1992. Effect of mutual shading on the emergenceof nodal roots and the root/shoot ratio of maize. Plant and Soil 147, 87–93.

bwongu, M., Adipala, E., Ssekabembe, C.K., Kyamanywa, S., Bhagsari, A.S., 2001.

Effect of intercropping maize and Solanum potato on yield of the componentcrops in Central Uganda. African Crop Science Journal 9, 83–96.

ournier, C., 2000. Modelisation des interactions entre plantes au sein des peuple-ments. Application a la simulation des regulations de la morphogenese aeriennedu maıs (Zea mays L.) par la competition pour la lumiere. Ph.D. Thesis. InstitutNational Agronomique Paris-Grignon, France.

W

W

xperimental Botany 64 (2008) 180–188

ibson, K.D., Foin, T.C., Hill, J.E., 1999. The relative importance of root and shootcompetition between water-seeded rice and Echinochloa phyllopogon. WeedResearch 39, 181–190.

ilbert, R.A., Heilman, J.L., Juo, A.S.R., 2003. Diurnal and seasonal light transmissionto cowpea in sorghum–cowpea intercrops in Mali. Journal of Agronomy and CropScience 189, 21–39.

irardin, P., 2000. Ecophysiologie du maıs. Association Generale des Producteurs deMaıs, France.

regory, P.J., Simonds, L.P., 1992. Water relations and growth of potatoes. In: Harris,P. (Ed.), The Potato Crop: The Scientific Basis for Improvement, 2nd ed. Chapman& Hall, London, UK, pp. 214–246.

all, M.R., Swanton, C.J., Anderson, G.W., 1992. The critical period of weed controlin grain corn. Weed Science 28, 441–447.

fekwe, O.P., Odurukwe, S.O., Okonkwo, J.C., Nwokocha, H.N., 1989. Effects of maizeand potato populations on tuber and grain yields, net income and land equivalentratios in potato/maize intercropping. Tropical Agriculture 66, 329–333.

wana, K., 1998. Development of nodal and lateral roots in potato under field condi-tions. Journal of the Faculty of Agriculture, Hokkaido University 68, 33–44.

wana, K., Nakaseko, K., Gotoh, K., Nishibe, S., Umemura, Y., 1979. Varietal differencesin root system and its relationship with shoot development and tuber yield.Japanese Tropical Crops Science 49, 495–501.

ropff, M.J., Weaver, S.E., Smits, M.A., 1992. Use of ecophysiological models forcrop-weed interference: relations amongst weed density, relative time of weedemergence, relative leaf area and yield loss. Weed Science 40, 296–301.

edent, J.F., Mouraux, D., 1990. Determination of foliar stage and number of leavesin maize when lower leaves are missing. Agronomie 2, 147–156.

i, L., Sun, J., Zhang, F., Li, X., Rengel, Z., Yang, S., 2001. Wheat/soybean strip intercrop-ping. II. Recovery or compensation of maize and soybean after wheat harvesting.Field Crops Research 71, 173–181.

iedgens, M., Soldati, A., Stamp, P., 2004. Interactions of maize and Italian ryegrassin a living mulch system: (1) shoot growth and rooting patterns. Plant and Soil262, 191–203.

ittell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., 1996. SAS© System for MixedModels. SAS Institute Inc., USA.

iu, J., Midmore, D.J., 1990. A review of potato intercropping practices in WesternHubei, China. Field Crops Research 25, 41–50.

idmore, D.J., 1990. Scientific basis and scope for further improvement of intercrop-ping with potato in the tropics. Field Crops Research 25, 3–24.

idmore, D.J., Roca, J., Barios, D., 1988. Potato (Solanum spp.) in the hot tropics. IV.Intercropping with maize and the influence of shade on microenvironment andcrop growth. Field Crops Research 18, 141–157.

’Brien, P.J., Firman, D.M., Allen, E.J., 1998. Effects of shading and seed tuber spacingon initiation and number of tubers in potato crops (Solanum tuberosum). Journalof Agricultural Science 130, 431–449.

zier-Lafontaine, H., Bruckler, L., Lafolie, F., Tournebize, R., Mollier, A., 1999.Modelisation de la competition pour l’eau dans une association culturale: influ-ence de la distribution des racines, des proprietes physiques du sol et de larepartition de la demande climatique. In: Maillard, P., et Bonhomme, R. (Eds.),Fonctionnement des peuplements vegetaux sous contraintes environnemen-tales. Les Colloques INRA, Paris, pp. 459–480.

ellerin, S., 1991. Effet d’une reduction du rayonnement incident sur l’emission desracines adventives du maıs en debut du cycle. Agronomie 11, 9–16.

ajcan, I., Swanton, C.J., 2001. Understanding maize–weed competition: resourcecompetition, light quality and the whole plant. Field Crops Research 71,139–150.

eed, A.J., Singletary, G.W., 1989. Roles of carbohydrate supply and phytohormonesin maize kernel abortion. Plant Physiology 91, 986–992.

obinson, D., 1996. Resource capture by localized root proliferation: why do plantsbother? Annals of Botany 77, 179–185.

odrigo, V.H.L., Stirling, C.M., Teklehaimanot, Z., Nugawela, A., 2001. Intercroppingwith banana to improve fractional interception and radiation-use efficiency ofimmature rubber plantations. Field Crops Research 69, 237–249.

ale, P.J.M., 1976. Effect of shading at different times on the growth and yield of thepotato. Australian Journal of Agricultural Research 27, 557–566.

choper, J.B., Johnson, R.R., Lambert, R.J., 1982. Maize yield response to increasedassimilate supply. Crop Science 22, 1184–1189.

etter, T.L., Flannigan, B.A., Melkonian, J., 2001. Loss of kernel set due to water deficitand shade in maize: carbohydrate supplies, abscissic acid, and cytokinins. CropScience 41, 1530–1540.

ouza, C.F., Matsura, E.E., 2003. Multi-wire time domain reflectometry (TDR) probewith electrical impedance discontinuities for measuring water content distri-bution. Agricultural Water Management 59, 205–216.

ournebize, R., Sinoquet, H., 1995. Light interception and partitioning in ashrub/grass mixture. Agricultural and Forest Meteorology 72, 277–294.

ander zaag, P., Demagante, A.L., 1990. Potato (Solanum spp) in an isohyper-thermic environment. V. Intercropping with maize. Field Crops Research 25,157–170.

allace, J.S., 1995. Towards a coupled light partitioning and transpiration model for

of Tropical Intercropping. INRA, Paris, pp. 153–162.ilson, S.D., 1988. Shoot and root competition. Journal of Applied Ecology 25,

279–296.ilson, S.D., Tilman, D., 1995. Competitive responses of eight old-field plant species

in four environments. Ecology 76, 1169–1180.