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Effects of environment and sowing date on the competition between faba bean (Vicia faba) and the parasitic weed Orobanche crenata
Field Crops Research 93 (2005) 300–313 www.elsevier.com/locate/fcr
Effects of environment and sowing date on the competition between faba bean (Vicia faba) and the parasitic weed Orobanche crenata J.H Grenza,*, A.M Manschadib, F.N Uygurc, J Sauerborna a
University of Hohenheim (380), Plant Production and Agroecology in the Tropics and Subtropics, Garbenstrasse 13, 70593 Stuttgart, Germany b Agricultural Production Systems Research Unit, DPI, Toowoomba, Australia c University of Cukurova, Department of Plant Protection, 01330 Adana, Turkey
Received 13 August 2004; received in revised form 2 November 2004; accepted 2 November 2004
Abstract In field trials conducted in southern Turkey during two growing seasons, effects of environment and management on the host–parasite association faba bean (Vicia faba)—Orobanche crenata were quantified. Experimental factors in each experiment included two sowing dates one to two months apart, parasite seedbank densities of 0, 25 and 200 seeds kg1 soil and two susceptible faba bean cultivars. In all treatments, parasitism had minor effects on faba bean vegetative growth. Reductions of stem dry weight occurred in infected crops during grainfilling and were most likely related to increased assimilate retranslocation. Up to 271 parasites m2 attached to the roots of the host, accumulating a maximum biomass of 701 g m2. Parasite number per host was a function of seedbank density and host root length density (RLD) in the top 15 cm of soil. Delayed sowing reduced the combined dry weight accumulation of host and parasite, which was not affected by parasite infection. Pod yield of faba bean ranged from 132 to 1019 g m2 and was affected by pedoclimatic conditions, sowing date and parasite infection. Parasitism mainly decreased host yield by reducing pod number. Seed size decreased to a lesser extent, while seed number per pod was not affected by parasite attack. Timing of host and parasite development phases, namely of the critical phase for faba bean pod setting, strongly affected host–parasite interactions and had decisive influence on the assimilate competition between pods and parasites. Via effects on host and parasite phenology, delayed sowing improved the relative competitive ability of pods during the critical phase, leading to lower parasite number and dry weight. As a consequence, reductions in combined host and parasite dry weight associated with delayed sowing mainly occurred at the expense of parasites. These findings may be transferred into specific control measures aimed at minimising the relative competitive ability of O. crenata during faba bean pod setting. # 2004 Elsevier B.V. All rights reserved. Keywords: Faba bean; Orobanche crenata; Sowing date; Competition; Partitioning; Yield formation
* Corresponding author. Tel.: +49 711 459 3601; fax: +49 711 459 3843. E-mail address: [email protected] (J. Grenz). 0378-4290/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2004.11.001
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1. Introduction Parasitic weeds belonging to the broomrape family (Orobanchaceae) frequently cause massive yield losses to agricultural crops (Parker and Riches, 1993). Central features of broomrape infestation include host specificity, connection to the vascular system of the host plant via a haustorium and a highly persistent soil seedbank (Cubero and Moreno, 1979; Stewart and Press, 1990). One of the most destructive species is Orobanche crenata (crenate broomrape), which inflicts considerable damage upon the production of faba bean (Vicia faba), lentil (Lens culinaris), chickpea (Cicer arietinum), pea (Pisum sativum) and other crops in Mediterranean countries (Sauerborn, 1991). This is all the more detrimental since these food legumes play a major role in providing high value protein in a balanced diet for the people of the affected region. Furthermore, N inputs from biological fixation by legumes are fundamental to sustainable crop production in Mediterranean agricultural systems (Howieson et al., 2000). Much effort has been invested in investigating impacts of O. crenata on host yields, clarifying biochemical aspects of host–parasite interactions and developing control methods (Sauerborn et al., 1989; Foy et al., 1989; Linke, 1992; to cite just a few). Yet none of the tested control measures has proven both effective and economically feasible mainly due to the complexity of host–parasite interactions. An integrated management strategy combining several approaches is most likely to provide durable control of the parasite (Linke and Saxena, 1991a). However, the development of integrated weed management strategies requires quantitative insight into the behaviour of the system under consideration (Kropff and Lotz, 1992). Quantitative information on O. crenata was collected in several studies. Phenological development of the parasite was found to be a function of soil temperature (Arjona-Berral et al., 1987; Sauerborn, 1989). The level of infection mainly depends on parasite seedbank density, degree of host genotype susceptibility to parasitism (Rubiales et al., 2003a) and the host root system (ter Borg and van Ast, 1991; Manschadi et al., 1997). In a field experiment in Syria, Manschadi et al. (2001) demonstrated that O. crenata infecting faba bean mainly grows at the expense of pods that have not yet reached the
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grainfilling phase. They then derived a framework of equations describing growth and development of host and parasite. It is not yet clear whether the described mechanisms are truly generic and can thus be extrapolated to other situations than those studied. Aspects of the interaction, such as N dynamics and the mechanisms causing host-yield reduction, remain unaccounted for. Effects of crop sowing date, specifically the mechanisms involved in the reductions of infection level often found in late-sown host crops (Mesa-Garcı´a and Garcı´a-Torres, 1986; Rubiales et al., 2003b), require further investigation. This study was designed to describe the growth kinetics of the association faba bean—O. crenata as affected by parasite infestation level and crop sowing date under a range of environmental conditions. Objectives were to (i) substantiate existing assumptions about the host–parasite association under different pedoclimatic conditions; (ii) understand the dynamics of assimilate competition between host and parasite and elucidate which growth and development processes are affected and (iii) quantify and explain these processes.
2. Material and methods 2.1. Experimental design Data were collected from on-station trials conducted at the University of Cukurova in Adana (Turkey) in the 2000–2001 and 2001–2002 growing seasons. Experiments were established at two locations per season: Balcali and Yumurtalik in 2000– 2001 and Balcali and Hacihasan in 2001–2002 (Table 1). The experimental station at Balcali is located in the centre of the Cukurova, an alluvial plain in southern Turkey. The parallel trials were situated close to the coast of the Mediterranean. Experiments were set up in a randomised split-split-plot design with four replications, with seedbank levels (SBL) of 0, 25 and 200 viable O. crenata seeds kg1 dry soil as main plot, two faba bean sowing dates per trial as subplot and two faba bean genotypes per trial as sub-subplot (Table 2). Genotypes sown included cultivar ILB 1814 (Syrian Local Large) and the Spanish cultivar Aquadulce, seeds of which were kindly provided by the International Center for Agricultural Research in
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Table 1 Climate and soil characteristics of the experimental locations Location
Coordinates
Rainfalla (mm)
Temperaturea (8C)
Soil type (FAO)
Soil texture
PAWC90b (mm)
pH
Balcali Hacihasan Yumurtalik
37.08N 35.48E 36.68N 35.48E 36.88N 35.88E
648 756 800
18.7 18.8 18.7
Chromic Cambisol Gleyic Cambisol Eutric Cambisol
Loamy clay Silty loam Sandy loam
195 210 149
7.4 8.4 7.7
a b
Long term (25 years) annual sum or average, respectively. Plant-available water capacity to 90 cm depth.
Table 2 Trial years, locations and factor levels in the experiments Trial
Year
Location
Infestation
1 2 3 4
2000–2001 2000–2001 2001–2002 2001–2002
Balcali Yumurtalik Balcali Hacihasan
0, 0, 0, 0,
a
25, 25, 25, 25,
200a 200 200 200
Sowing dates
Cultivars
Dec-1, Jan-4 Dec-2, Jan-6 Nov-5, Dec-13 Nov-8, Jan-26
ILB 1814, Sakiz ILB 1814, Sakiz Aquadulce, Sakiz Aquadulce, Sakiz
Viable O. crenate seeds kg1 soil.
the Dry Areas (ICARDA) at Aleppo (Syria), and the local variety Sakiz. Thousand seed weights (TSW) were 1300, 1150 and 800 g, respectively. None of these genotypes has been reported to display any resistance to O. crenata infection. Faba bean was manually sown at a density of 20 seeds m2 with 50 cm row spacing and 5 cm sowing depth. Prior to sowing, plots were artificially infested with parasite seeds at the desired densities to a depth of 15 cm. No previous Orobanche spp. infestations existed in the fields, thus, controls could be created by leaving parcels noninfested. Parasite seed viability was determined to be 60% by triphenyl–tetrazolium– chloride test (Linke and Saxena, 1991b). The applied total inoculum was therefore 42 and 333 seeds kg1 dry soil, equal to 25.2 and 199.8 mg seeds m2. Broomrape seeds and fertiliser (diammonium-phosphate) were incorporated into the top 15 cm of soil at rates of 20 kg N and 50 kg P2O5 ha1 by use of a rotivator. Insect pests and fungal diseases were controlled chemically (deltamethrin, iprodione), while weeds were removed by repeated hoeing. After the final harvest, crop and parasite residues were burnt and the soil thoroughly harrowed and irrigated. Then the field was solarised by covering it with clear polyethylene sheets during six weeks in July and August to ensure no viable parasite seeds would remain.
2.2. Data collection Air temperature, soil temperature in 10 cm depth, rainfall and global radiation were continuously recorded by weather stations (m-Metos, Pessl Instruments, Austria) installed in the fields. Soil moisture down to 90 cm depth was measured fortnightly in four profiles per location using a time domain reflectometry tube probe system (IMKO, Germany) in the first and the gravimetric method in the second season. The phenological development of host and parasite was recorded weekly. Faba bean phenology was rated using the key of Knott (1990). Sequential biomass harvests as described by Manschadi et al. (2001) were carried out at four-week intervals, starting three weeks after faba bean emergence, to quantify plant organ numbers and dry weights. All broomrapes attached to the sampled faba bean plants were dug out with a spade to 20 cm depth, counted and their dry weight determined. At each biomass harvest, four to six soil monoliths (Bo¨ hm, 1979), 8 cm in diameter and 15 cm high, were taken to 45 cm depth beneath and beside one plant in each noninfested plot. Samples were soaked in water for dispersal and washed over a 1 mm sieve. Roots were scanned, root length measured using the WinRhizoTM program (Re´ gent Instruments, Canada) and root dry weight determined. In the second season, aliquots of all samples were stored in
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airtight bags. Approximately 3 g of each sample were ground in a steel mill and total N content analysed by Dumas dry combustion technique. 2.3. Statistical analysis The concept of thermal time (Ritchie and NeSmith, 1991) was applied to relate events to each other. Thermal time calculations for crop and parasite development from crop sowing and parasite germination to host and parasite emergence, respectively, were based on measured soil temperatures. Base temperatures of 0 8C and 4 8C were assumed for faba bean and O. crenata, respectively (Sauerborn, 1989; Manschadi et al., 2001). Analysis of variance was performed using the General Linear Model procedure of the MiniTabTM (release 13.20, MiniTab Inc.) statistical package. Differences between means were tested for significance by Tukey test (p 0.05). For regression calculations, the SigmaPlotTM (Version 6.00, SPSS Inc.) statistical program was used. For analysis of parasite attachment number, our data were first analysed separately and then pooled with results of Manschadi et al. (2001) to cover a wider range of environmental conditions. Regression analysis had shown the same function types to apply to both data sets. Where genotype differences were nonsignificant, cultivar results were pooled. Parasite numbers and dry weights in trial 4 deviated from the pattern found in the other trials, and parasite development was delayed. Inferring from the similar experience of Manschadi
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et al. (2001), we reasoned that parasite seeds had not been properly incorporated into the soil. Results from infested plots in trial 4 were therefore excluded from analysis. However, weather and soil conditions in this trial resulted in yields of parasite-free plots ranking among the highest ever reported for faba bean. Since data illustrating the potential growth of rainfed faba bean under Mediterranean conditions are rare, results from noninfested plots of trial 4 will be presented here.
3. Results 3.1. Weather conditions In 2000–2001, early-sown crops received 213 mm of rainfall in Balcali and 559 mm in Yumurtalik. In 2001–2002, 756 mm precipitation were measured in Balcali and 812 mm in Hacihasan. Intensive rainfalls in Hacihasan lead to some waterlogging in December 2001, which the crop tolerated well. Temperatures were in the range of the long-term regional average during both growing seasons. Neither frost spells nor excessively high temperatures occurred (Fig. 1). 3.2. Host and parasite phenology Faba beans emerged approximately 300 8C d after sowing, water and cold stress caused some delay. Development from emergence to flowering was accelerated in late-sown crops. The duration of the
Fig. 1. Average monthly temperature (bold line), monthly rainfall (columns) and plant-available soil water from 0 to 90 cm depth (dashed line with symbols) at the experimental locations.
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Table 3 Thermal duration of V. faba and O. crenata development phases in degree-days (8C d) as affected by environmental conditions and sowing date Phase
V. faba sowing– V. faba emergence V. faba emergence– V. faba flowering V. faba flowering– V. faba maturity V. faba emergence– O. crenata emergence
Balcali 2000–2001
Yumurtalik 2000–2001
Balcali 2001–2002
Hacihasan 2001–2002
December 1
December 2
November 5
November 8
January 4
January 6
December 13
January 26
293
266
383
290
416
246
245
235
749
647
738
566
755
743
914
650
1081
945
1216
1152
1577
1406
1453
1122
844
847
764
735
771
784
Figures for V. faba were averaged across genotypes. Thermal time calculations for O. crenata were done using a base temperature of 4 8C.
phase from flowering to physiological maturity displayed the greatest variability and was affected by sowing date and moisture supply. Parasitism caused a shortening of grainfilling by 50–200 8C d, depending on the degree of infection. The period from faba bean emergence, when the first O. crenata seeds can be expected to have been stimulated by root exudates (Linke, 1987), until parasite emergence varied little across trials and treatments (Table 3). 3.3. V. faba stem, leaf and root growth Tiller formation initially progressed at a rate of one additional tiller per 200 8C d, then slowed down, and during grainfilling, stem number was often reduced. Total and per tiller stem weight, but not tiller number, were reduced by delayed sowing in all genotypes. Infection with O. crenata did not affect tiller
formation, but significantly decreased total and per tiller stem weight. Effects of parasitism on stem growth appeared at the start of grainfilling and became significant at mid-grainfilling (Fig. 2). In the most severely infected crop, maximum stem weight was reduced by 46% (trial 3, sowing date 1, Aquadulce) as compared to the control. At physiological maturity, stem N concentration in early-sown crops was 0.8% in noninfected and 0.5% in severely infected faba bean (Fig. 3). Leaf numbers increased at an average rate of one per 32 8C d until grainfilling. Maximum leaf numbers were 50–55 per plant in all three genotypes and were found in early-sown treatments. Parasite infection caused non-significant reductions of leaf number and area (Fig. 4). Leaf N concentration prior to shedding of the last leaves was 3.4% in early-sown noninfected and 2.4% in severely infected faba bean (Fig. 3).
Fig. 2. Course of faba bean stem dry weight under different pedoclimatic conditions as affected by O. crenata infection. Symbol meanings: (*) noninfested control, (&) infested with 25 broomrape seeds kg1 soil, (~) infested with 200 broomrape seeds kg1 soil. E: host emergence; F: flowering; OE: parasite emergence; OM: maturity of infected crops; M: maturity of noninfected crops. Similar courses were obtained from the other locations and sowing dates.
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Fig. 3. Total N concentration in faba bean organs and in O. crenata. Symbol meanings: (*) stem; (& ) green leaf; (~) seed; (^) parasite. Full symbols represent nonparasitised control, hollow symbols treatments infested with 200 viable O. crenata seeds kg1 soil.
Fig. 4. Leaf area index (LAI) of faba bean as affected by sowing date and O. crenata infection (symbol meanings as in Fig. 2).
Faba bean roots were concentrated in the top 15 cm, where mean root length density (RLD) peaked at 2.2–2.3 cm cm3 both beneath and beside plants. RLD was highest in early-sown treatments and crops with good water supply. Root development was more vigorous in 2001–2002 than in 2000–2001. Delayed sowing caused a reduction of maximum RLD in the top 15 cm. 3.4. V. faba shoot growth Growth of faba bean shoots (green, standing, above-ground plant parts) was strongly affected by soil moisture content. The maximum dry weight of noninfected crops sown at Balcali in December 2001 exceeded that of faba bean sown in December 2000 by 23.9%. Shoot dry weight peaked at 488–920 g m2 in
2000–2001, and at 786–1721 g m2 in 2001–2002. Most crops experienced a net loss of shoot biomass from mid-grainfilling until maturity due to leaf senescence and detachment. Trends of shoot N accumulation paralleled those of total shoot growth, with a distinct peak during early grainfilling. Retarded sowing resulted in a shorter growing period, lower growth rates, and consequently less shoot dry weight. Delay by one month reduced the final dry weight of nonparasitised shoots by 10 (trial 3) to 34% (trial 1) (Table 4). In parasitised crops, the biomass reduction caused by delayed sowing mainly occurred at the expense of parasites (Fig. 5). During grainfilling, parasite growth rate often exceeded the combined growth rate of host and parasites, indicating retranslocation from stems and leaves to O. crenata. Parasite infection did not significantly alter combined
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Table 4 Mean values with standard errors () of maximum faba bean shoot dry weight (DW), leaf area index and pod dry weight, as well as O. crenata dry weight and number in crops infested with 0, 25 and 200 O. crenata seeds (OC) kg1 soil, respectively (all weights in g m2) Trial
OC 0
OC 25
OC 200
Sowing date
Faba bean shoot DW
Faba bean LAI
Faba bean pod DW
Faba bean pod DW
Faba bean pod DW
1
1 2
992.9 84.28 645.9 36.03
3.8 0.52 2.1 0.16
495.9 47.89 337.5 15.66
401.2 34.03 285.6 17.54
156.6 26.10 187.1 18.49
2
1 2
1014.0 44.16 742.7 42.85
2.8 0.32 3.2 0.29
637.8 23.68 410.9 29.74
498.6 83.27 383.3 53.89
131.6 30.62 226.3 41.85
3
1 2
1480.7 36.77 1303.4 60.86
4.5 0.21 4.4 0.36
888.8 52.34 869.4 62.95
667.5 77.51 511.9 61.28
165.0 26.44 179.4 34.13
4
1 2
1633.0 80.71 1065.9 48.31
6.0 0.36 5.4 0.32
1019.3 40.55 615.7 35.21
Trial
Sowing date
OC 25, parasite DW
OC 200, parasite DW
OC 25, parasite population
OC 200, parasite population
1
1 2
107.23 20.86 38.43 5.48
265.5 19.00 124.3 11.46
23.8 2.52 14.5 3.52
91.0 9.16 43.3 2.42
2
1 2
114.9 27.27 64.2 9.11
366.4 50.37 171.6 32.31
30.5 6.25 13.0 2.88
115.8 16.84 48.5 12.25
3
1 2
363.5 60.03 214.4 23.15
700.7 66.57 415.6 26.49
77.8 12.55 34.6 5.57
270.6 21.30 151.4 15.13
host and parasite biomass until mid-grainfilling (Fig. 6). Towards maturity, combined host–parasite biomass rapidly decreased in early-sown treatments, leading to lower biomass at harvest as compared to noninfected crops. Parasites accounted for most of the loss by maturing and decomposing earlier than faba bean. At harvest, O. crenata accounted for 50–64% of the combined host–parasite biomass in severely infected
crops. Parasitism also affected amount and composition of harvest residues. Since pods were collected, while parasites remained in the field, total residue weight of infected crops was up to 111% more and residue N up to 72% more than in noninfected faba bean. Severe broomrape infection reduced total N accumulation by up to 52% in 2001–2002. Linear
Fig. 5. Maximum dry weights of faba bean organs and O. crenata at a seedbank density of 200 viable O. crenata seeds kg1 soil as affected by sowing date (black columns: early, grey columns: late; for exact dates see Table 2) under different pedoclimatic conditions.
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Fig. 6. Combined biomass of faba bean and O. crenata as affected by parasite infection under contrasting weather and soil conditions (symbol meanings as in Fig. 2).
regression analysis showed variations in N accumulation to be related to altered assimilate partitioning (r2 = 0.64), not to reduced organ N concentrations (r2 = 0.05). There were no consistent genotype effects on maximum or final values of shoot dry weight or organ N concentrations. 3.5. O. crenata infection and growth Parasite numbers presented here refer to visible O. crenata attachments, both emerged and nonemerged. Parasite numbers varied from 13 to 271 m2, equalling 0.7–13.6 per host plant. Increased shoot dry weight caused by better moisture supply, as in trial 3, resulted in higher parasite numbers and dry weight (Table 4). Delaying sowing by one month reduced parasite numbers in plots infested with 200 viable parasite seeds kg1 soil by 52, 58 and 44% in trials 1, 2 and 3, respectively. Results of Manschadi et al. (2001), who collected data from faba bean cultivar ILB 1814 grown at infestation levels of 50, 200 and 600 viable O. crenata seeds kg1 soil in northwest Syria, were included in the following analysis to expand the range of conditions. Response functions of parasite number to the variables considered were similar in our experiments and those of Manschadi et al. (2001). Attachment number mainly was a function of parasite seedbank level and maximum host RLD in 0–15 cm depth. Parasite numbers increased up to a RLD of slightly above 2.0 cm cm3. Since effects of RLD ceased beyond that level, regression analysis of parasite number as affected by SBL was only
performed for treatments where RLD exceeded 2.1 cm cm3. A rectangular hyperbolic function yielded the best fit (Fig. 7, left). Effects of RLD on attachment number were analysed for treatments with SBL of 200 seeds kg1 soil, since this level was included in all trials. The best fit was achieved by a sigmoidal function (Fig. 7, right). Assuming no mutual interactions between SBL and RLD, the hyperbola was linearly transformed and multiplicatively coupled with the sigmoidal function. Linear regression of calculated against observed parasite numbers showed the resulting two-factorial equation P ¼ 307:1=ð1þ eððRLD-1:49Þ=0:41Þ Þð3:8 SBL=ð552:46 þ SBLÞÞ
where P (parasites m2) is a function of RLD (cm cm3) and SBL (viable seeds kg1 soil, 0–15 cm depth), to explain 95% of the observed variation in maximum parasite number. In severely infected crops, final parasite number was less than 50% of the maximum, since many attachments died before emergence. Parasite growth was rapid, average daily growth rates during faba bean grainfilling reached up to 1.17 g m2 8C d1, equaling 230 kg ha1 d1. Maximum O. crenata dry weight was 366 g m2 in 2000– 2001 and 701 g m2 in 2001–2002 (Table 4). Average individual parasite dry weight was negatively correlated with attachment number, but was not affected by sowing date or cultivar. Total N concentration in O. crenata tissue was close to 2% across trials, treatments and development stages (Fig. 3).
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Fig. 7. Maximum O. crenata attachment number as affected by parasite seedbank density in treatments with maximum faba bean root length density above 2.1 cm cm3 (left) and as affected by maximum faba bean root length density at a seedbank density of 200 viable O. crenata seeds kg1 soil (right). Symbol meanings: (*) experiments described in Table 2; (~) experiments of Manschadi et al. (2001).
3.6. V. faba yield formation Faba bean pod dry weight at harvest ranged from 132 to 1019 g m2 (Table 4), seed dry weights varied between 101 and 831 g m2. Seeds accounted for 80% and husks for 20% of pod weight, with no significant variations across trials and treatments. All findings on pod yield presented here similarly apply to seed yield. Pod and seed yield were significantly affected by all experimental factors. When sowing was delayed by one month, the pod yield of noninfected faba bean decreased by 32, 36 and 2% in trials 1, 2 and 3, respectively. In parasitised plants, pod growth was slowed down, while combined pod and parasite dry weight increased at the same rate as in noninfected crops. Parasitism on average reduced pod yield by 25 and 71% at infestation rates of 25 and 200 viable parasite seeds kg1 soil. The response curve of pod yield to the number of O. crenata attachments followed a hyperbolic decay function (Fig. 8). Delayed sowing diminished crop yield loss caused by O. crenata. In parcels infested with 200 viable parasite seeds kg1 soil, average yield loss due to parasitism was 81.4, 72.3 and 45.9% in crops sown in November (trial 3, sowing date 1), December (trials 1 and 2, sowing date 1; trial 3, sowing date 2) and January (trials 1 and 2, sowing date 2), respectively. Pearson correlations between pod yield and factors of yield formation were +0.299 for TSW, +0.247 for the number of seeds per pod, and +0.884 for pod number per m2. Linear regression showed pod number
Fig. 8. Relative faba bean pod yield, calculated as fraction of the yield measured in the respective noninfected control, as affected by O. crenata attachment number. Symbol meanings: (*) trial 1; (^) trial 2; (& )trial 3 (see Table 2).
to explain 74.7, 76.6 and 80.4% (r2) of observed variations in pod yield in trials 1, 2 and 3, respectively. The respective figure for the combined data sets was 73.6% (Fig. 9). Adding seeds per pod and TSW to the regression equation increased r2 to 88.5, 93.1 and 97.4%, respectively. Pod number was significantly reduced by delayed sowing and by parasitism. The effect of O. crenata infection set on at podsetting and was significant across locations, sowing dates and cultivars. Seed number per pod significantly differed between genotypes and responded negatively to delayed sowing, but not to parasitism. Delayed sowing resulted
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Reductions of total seed N in infected crops reached 89% and were mainly related to reduced seed dry weight (r2 = 0.95), not to lower seed N concentration. See Table 5 for a comprehensive summary of consistent effects of experimental factors on faba bean and O. crenata growth and development.
4. Discussion 4.1. Determinants of O. crenata infection
Fig. 9. Effect of pod number on pod yield: relative faba bean pod yield, with the yield of nonparasitised treatments set 1.0, as affected by relative pod number (symbol meanings as in Fig. 8).
in significantly reduced TSW in the control treatments. Infestation with 200 parasite seeds kg1 soil caused reductions of TSW by 30.8, 27.7 and 20.9% in early-sown, and by 6.3 (increase), 22.2 and 21.4% in late-sown treatments of trials 1, 2 and 3, respectively. There was a significant interaction between effects of delayed sowing and parasitism on TSW. Severe parasite attack reduced final seed N concentration of early-sown faba bean from 4.2 to 3.7% (Fig. 3).
The extent of O. crenata effects on host growth is a function of parasite number and assimilate demand per parasite (Manschadi et al., 2001). The main determinant of parasite number at given SBL was maximum RLD, which is in accordance with previous findings (ter Borg and van Ast, 1991; Manschadi et al., 2001). The response of parasite number to RLD followed a sigmoidal curve approaching an asymptote at RLD of 2.0–2.5 cm cm3. Parasite stimulation depends on the presence of a host root less than 2 mm from the seed (Linke and Vogt, 1987), hence it is plausible that the number of stimulated broomrape seeds rises with increasing RLD. The asymptote marking complete stimulation of the seedbank was lower at high values of SBL, most likely due to
Table 5 (a) Effects of parasite infestation, sowing date and genotype consistent (p 0.05, General Linear Model) across trials 1, 2 and 3 Parasite infestation
Sowing date
Genotype
Postflowering development (+) Maximum crop standing DW () Stem DW at harvest () Pod No at harvest () Pod DW at harvest () Maximum parasite No (+) Maximum parasite DW (+) Mean DW per parasite ()
Preflowering development (+) Postflowering development (+) Maximum crop standing DW () Maximum system DW () (=crop + parasite) Stem DW at harvest () Maximum parasite No () Maximum parasite DW ()
Stem DW at harvest (Sakiz < ILB1814/Aquadulce) Mean seed DW at harvest (Sakiz < ILB1814/Aquadulce) Mean seed No per pod (Sakiz > ILB1814/Aquadulce)
(b) Variables consistently not affected by parasite infestation, sowing date or genotype (p 0.05, General Linear Model) across trials 1, 2 and 3 Preflowering development Maximum stem No Maximum crop standing DW Maximum system DW Pod No at harvest Maximum system DW Maximum stem No Mean seed No per pod Maximum stem No Maximum leaf/node No Maximum leaf No Maximum leaf DW Maximum leaf DW Mean seed No per pod Maximum parasite No Maximum parasite DW Mean DW per parasite Symbol meanings: (+): increased growth/accelerated development at higher infestation level/delayed sowing; (): reduced growth or slower development; (DW): dry weight; (No): number.
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intraspecific competition. The response of attachment number to SBL followed a hyperbola nearly linear at low, but asymptotic at high levels of infestation. This asymptotic curve is typical for density-dependent functions (Naylor, 2002) and reflects intraspecific competition. This may also explain why many parasites did not emerge when population density was high. Furthermore, average parasite dry weight was lower in severely infected crops. Other factors that can affect attachment number, such as fatal germination due to low soil temperature (Sauerborn, 1989) and resistance mechanisms leading to reduced establishment of attachments (Rubiales et al., 2003a), did not seem to play a role in our experiments. Our results suggest that at the given sowing density, one plant of faba bean cultivar ILB 1814 or Aquadulce growing under near-optimal conditions can support either about 10 well-developed pods or 10 to 15 full-grown O. crenata individuals until physiological maturity. This carrying capacity of the crop is a function of biomass accumulation, which in turn depends on pedoclimatic conditions and sowing date. 4.2. Effects of parasitism on V. faba Within the range of conditions encountered, O. crenata infection had no effects on the vegetative growth phase of faba bean, which is in accordance with findings of Mesa-Garcı´a and Garcı´a-Torres (1984). Parasitism had minor influence on size and functionality of the host leaf apparatus, thus on assimilative capacity. Accordingly, the combined growth of host and parasite did not differ from that of noninfected crops, as also observed by Manschadi et al. (1996). The only significant effect of parasitism on vegetative growth was a reduction of stem biomass during grainfilling. This indicates increased retranslocation of assimilate to parasites, which explains how parasites could grow at faster rates than host and parasites combined. Effects of parasitism on host N metabolism were weak. Minor reductions of N concentration affected stems, leaves and seeds during grainfilling. Replacement of pods containing 4% N by parasites with only 2% N resulted in lower system N accumulation. Contrary to findings of el-Ghamrawy and Neumann (1991), extremely reduced N concentrations did not affect any plant organ. Reduced N
uptake of infected crops was related to altered carbohydrate partitioning and testifies a dominance of C over N flows. While O. crenata did not disturb assimilate production, it massively altered the sink side of the assimilate balance. Biomass loss in the host mostly occurred at the cost of pods, which are the organs with which parasites mainly compete for assimilate (Manschadi et al., 1996). Yield of grain legumes is the product of pod number, seed number per pod and TSW (Egli, 1998). In faba bean, pod number is the major determinant of yield variations (e.g. Pilbeam et al., 1989; Adisarwanto and Knight, 1997; Loss and Siddique, 1997). Pod and seed number are a function of crop physiological status during a critical period (Jiang and Egli, 1995; Egli, 1998; Vega et al., 2001). In faba bean, this period begins around the start of flowering and lasts approximately 550 8C d (Stu¨ tzel and Aufhammer, 1992). Sink strength of legume pods during most of the critical period is proportional to organ biomass (Jeuffroy and Devienne, 1995, on pea). During this phase, reduced assimilate supply due to insufficient sink strength results in pod abortion (Egli and Bruening, 2001, on soybean (Glycine max)). During the subsequent grainfilling phase, when sink strength is at its maximum, pod and seed numbers are no longer subject to change (Egli, 1998). The time course of sink strength and biomass accumulation follows a sigmoidal pattern consisting of lag, linear and maturation phase in legume seeds and pods (Egli, 1998), as well as in O. crenata individuals (Manschadi et al., 2001). Parasitism reduced pod number and caused some reduction of TSW. Since pod number in parasitised crops was reduced from pod setting onwards, we can assume that pods and parasites started to compete for assimilate during the critical period. By developing faster and entering the linear growth phase earlier than pods, parasites accumulated sufficient sink strength to outcompete pods, which were aborted. Hence, the competitive abilities of pods and parasites during the critical period decided about their fate. Parasites then benefited from the inherent stability of the legume sink hierarchy. TSW results from rate and duration of seed growth. Its reduction was probably caused by a shortened grainfilling duration due to accelerated senescence.
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Lower faba bean TSW associated with shortened grainfilling was also reported by Loss and Siddique (1997) and Loss et al. (1997). Reduced seed growth rate is unlikely to have played a role, since it was shown by Munier-Joulain et al. (1998, on pea, lupin (Lupinus albus) and soybean) that even strongly reduced assimilate availability during grainfilling did not affect growth rates of legume seeds. The responsiveness of host–parasite interactions to shifted sowing date testifies the importance of the timing of host and parasite development stages, as reckoned by Manschadi et al. (1996). The biochemical adaptions that enable parasites to seize the place of pods as sinks for assimilate, with their distance from the source tissues obviously not imposing a problem, remain to be elucidated. Phytohormones are likely to play a role, since substances from the cytokinin group are important in the regulation of fruit production and abortion of legumes (Nagel et al., 2001; Liu and Longnecker, 2002). El-Ghamrawy and Neumann (1991) found applications of kinetin to the host apex to increase pod number in faba bean infected with O. crenata. Specific control measures should aim at minimising the competitive ability of parasites relative to that of pods during the critical period of legume pod setting. Assimilate allocation to pods can be stimulated by phytohormone applications (el-Ghamrawy and Neumann, 1991). Improving the timing of sowing, fertilisation and irrigation measures could help synchronise assimilate supply with the critical period of pods, but desynchronise it with the maximum demand of parasites. Alternatively, it might be possible to retard or disturb development and growth
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of parasites during the critical phase by herbicide application (Foy et al., 1989). Information on the likely occurrence of the critical period, which could be generated by simulation models, might help optimise the timing of such measures. 4.3. Effects of sowing date on host–parasite competition Delayed sowing resulted in reduced faba bean growth and yield, the latter of which was mainly associated with lower TSW. Late-sown crops are subjected to the senescence-accelerating heat and water stress of the Mediterranean summer at an earlier stage, which leads to a shorter grainfilling period. Correlations between shorter grainfilling phase and reduced TSW were also observed by Adisarwanto and Knight (1997) and Loss et al. (1997). The negative effect of delayed sowing on the level of O. crenata infection observed in previous studies (Mesa-Garcı´a and Garcı´a-Torres, 1986; Manschadi et al., 2001) was confirmed. Similar responses to delayed sowing were reported for O. crenata infecting carrot (Daucus carota) (Eizenberg et al., 2001), chickpea (Rubiales et al., 2003b) and pea (Rubiales et al., 2003c). Reduced parasite numbers and biomass in late-sown crops have mainly been attributed to effects of soil temperature on parasite development. Suboptimal temperatures are likely to cause a high percentage of fatal germination and a delay in parasite development (Sauerborn, 1989), while in crops sown in autumn, parasites may establish before the onset of cold temperatures (Rubiales et al., 2003b) and benefit
Fig. 10. Schematic representation of the effect of sowing date on phenological development of faba bean and O. crenata (S: sowing; E: emergence; F: flowering; P: pod setting; M: maturity; G: germination). The line in the background represents daylength. Arrows indicate the approximate start of pod and parasite linear growth, respectively. In late-sown crops, the competitive advantage of parasites is neutralised.
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from a head start relative to generative organs of the host in spring. Other factors that may affect host– parasite interactions include moisture supply, host RLD and photoperiod. In late-sown crops, development phases are shifted towards summer, when water supply becomes limiting. However, direct effects of moisture supply on parasite growth and development were not found. The observed reduction of parasite number in late-sown faba bean indeed went along with lower RLD, which may have resulted in a lower probability of parasite seed stimulation. However, the irrigated trials of Manschadi et al. (2001) showed that delayed sowing not always leads to reduced root growth, hence this mechanism is probably not generic. Photoperiod has major effects on crop phenology. Faba bean is a quantitative long-day plant responding to daylength during most pre- and postflowering development phases (Turpin et al., 2003). In the Mediterranean region, crops sown in autumn enter the photoperiod-sensitive phase of development when daylength is at its annual minimum. Delayed sowing corresponds with a shift to periods of longer days, leading to accelerated development. The development rate of O. crenata on the contrary is solely driven by ambient temperature (Manschadi et al., 2001). Late-sown faba bean reached flowering, hence the critical period, within less thermal time, while the duration of parasite development was constant across sowing dates and environments. Effects of drought stress accelerating faba bean development may have added to this difference. Faster development may allow late-sown faba bean to enter the phase of linear seed growth earlier and thus have higher sink strength than parasites during the critical period. Delayed sowing thus reduces or neutralises the head start in the competition for assimilate during the critical phase that parasites have in early-sown crops (Fig. 10). Consequently, relatively less pods and more parasites are aborted. Parasites are obviously unable to compensate for this advantage of the crop, neither by transmitting some biochemical signal nor by accelerating their own development.
Acknowledgement This work was financially supported by a scholarship of the German National Academic Foundation.
References Adisarwanto, T., Knight, R., 1997. Effect of sowing date and plant density on yield and yield components in the faba bean. Aust. J. Agric. Res. 48, 1161–1168. Arjona-Berral, A., Mesa-Garcı´a, J., Garcı´a-Torres, L., 1987. Phenology and growth of Orobanche crenata Forsk (broomrape) in four legume crops. Weed Res. 27, 349–360. Bo¨ hm, W., 1979. Methods of Studying Root Systems. SpringerVerlag, Berlin. Cubero, J.I., Moreno, M.T., 1979. Agronomical control and sources of resistance in Vicia faba to O. crenata. In: Bond, D.A., Scarascia-Mugnozza, G.T., Poulsen, M.H. (Eds.), Some current Research on Vicia faba in Western Europe. Commission of the European Communities, Luxemburg, pp. 41–80. Egli, D.B., 1998. Seed Biology and the Yield of Grain Crops. CAB International, Wallingford. Egli, D.B., Bruening, W.P., 2001. Source-sink relationships, seed sucrose levels and seed growth rates in soybean. Ann. Bot. 88, 235–242. Eizenberg, H., Tanaami, Z., Jacobsohn, R., Rubin, B., 2001. Effect of temperature on the relationship between Orobanche spp. and carrot (Daucus carota L.). Crop Prot. 20, 415–420. el-Ghamrawy, N., Neumann, K.H., 1991. Some physiological aspects of Orobanche crenata parasitism on Vicia faba. In: Wegmann, K., Musselman, L.J. (Eds.), Progress in Orobanche Research. Universita¨ t Tu¨ bingen, Tu¨ bingen, pp. 134– 146. Foy, C.F., Rakesh, J., Jacobsohn, R., 1989. Recent approaches for chemical control of broomrape (Orobanche spp.). Rev. Weed Sci. 4, 123–152. Howieson, J.G., O’Hara, G.W., Carr, S.J., 2000. Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crops Res. 65, 107–122. Jeuffroy, M.H., Devienne, F., 1995. A simulation model for assimilate partitioning between pods in pea (Pisum sativum L.) during the period of seed set; validation in field conditions. Field Crops Res. 41, 79–89. Jiang, H., Egli, D.B., 1995. Soybean seed number and crop growth rate during flowering. Agron. J. 87, 264–267. Knott, C.M., 1990. A key for stages of development of the faba bean (Vicia faba). Ann. Appl. Biol. 116, 391–404. Kropff, M.J., Lotz, L.A.P., 1992. Systems approaches to quantify crop-weed interactions and their application in weed management. Agric. Syst. 40, 265–282. Linke, K.H., 1987. Untersuchungen u¨ ber Keimung und Jugendentwicklung von Striga und Orobanche (in German), PLITS 1987/5 (3), Verlag Josef Margraf, Weikersheim. Linke, K.H., Vogt, W., 1987. A method and its application for observing germination and early development of Striga (Scrophulariaceae) and Orobanche (Orobanchaceae). In: Proceedings of the 4th International Parasitic Weed Symposium, Marburg, pp. 501–509. Linke, K.H., Saxena, M.C., 1991a. Towards an integrated control of Orobanche spp. in some legume crops. In: Wegmann, K., Musselman, L.J. (Eds.), Progress in Orobanche Research. Universita¨ t Tu¨ bingen, Tu¨ bingen, pp. 248–256.
J.H. Grenz et al. / Field Crops Research 93 (2005) 300–313 Linke, K.H., Saxena, M.C., 1991b. Study on viability and longevity of Orobanche seed under laboratory conditions. In: Wegmann, K., Musselman, L.J. (Eds.), Progress in Orobanche Research. Universita¨ t Tu¨ bingen, Tu¨ bingen, pp. 110–114. Linke, K.H., 1992. Biology and control of Orobanche in legume crops. PLITS 1992/10 (2), Verlag Josef Margraf, Weikersheim. Liu, F.H., Longnecker, N., 2002. Interactive effect of cytokinin and potassium on sink-source relationships in Lupinus angustifolius. Plant Growth Regul. 36, 1–6. Loss, S.P., Siddique, K.H.M., 1997. Adaptation of faba bean (Vicia faba L.) to dryland Mediterranean-type environments I. Seed yield and yield components. Field Crops Res. 52, 17–28. Loss, S.P., Siddique, K.H.M., Martin, L.D., 1997. Adaptation of faba bean (Vicia faba L.) to dryland Mediterranean-type environments II. Phenology, canopy development, radiation absorption and biomass partitioning. Field Crops Res. 52, 29–41. Manschadi, A.M., Kroschel, J., Sauerborn, J., 1996. Dry matter production and partitioning in the host–parasite association Vicia faba–Orobanche crenata. J. Appl. Bot. 70, 224–229. Manschadi, A.M., Sauerborn, J., Kroschel, J., Saxena, M.C., 1997. Effect of plant density on grain yield, root length density, and Orobanche crenata infestation in two faba bean genotypes. Weed Res. 37, 39–49. Manschadi, A.M., Sauerborn, J., Stu¨ tzel, H., 2001. Quantitative aspects of Orobanche crenata infestation in faba beans as affected by abiotic factors and parasite soil seedbank. Weed Res. 41, 311–324. Mesa-Garcı´a, J., Garcı´a-Torres, L., 1984. A competition index for Orobanche crenata Forsk. effects on broad bean (Vicia faba L.). Weed Res. 24, 379–382. Mesa-Garcı´a, J., Garcı´a-Torres, L., 1986. Effect of planting date on parasitism of broadbean (Vicia faba) by crenate broomrape (Orobanche crenata). Weed Sci. 34, 544–550. Munier-Joulain, N.G., Munier-Joulain, N.M., Roche, R., Ney, B., Duthion, C., 1998. Seed growth rate in grain legumes I. Effect of photoassimilate availability on seed growth rate. J. Exp. Bot. 49, 1963–1969. Nagel, L., Brewster, R., Riedell, W.E., Reese, R.N., 2001. Cytokinin regulation of flower and pod set in soybeans (Glycine max (L.) Merr.). Ann. Bot. 88, 27–31. Naylor, R.E., 2002. Weed population dynamics. In: Naylor, R.E. (Ed.), Weed Management Handbook. Blackwell Science, Oxford. Parker, C., Riches, C.R., 1993. Parasitic Weeds of the World: Biology and Control. CAB International, Wallingford.
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Pilbeam, C.J., Hebblethwaite, P.D., Ricketts, H.E., 1989. The response of determinate and semi-determinate faba bean varieties to different sowing dates in the spring. Ann. Appl. Biol. 114, 377–390. Ritchie, J.T., NeSmith, D.S., 1991. Temperature and crop development. In: Hanks, J., Ritchie, J.T. (Eds.), Modelling Plant and Soil Systems. ASA-CSSA-SSSA, Madison, pp. 5–29. Rubiales, D., Pe´ rez-de-Luque, A., Joel, D.M., Alca´ ntara, C., Sillero, J.C., 2003a. Characterization of resistance in chickpea to crenate broomrape (Orobanche crenata). Weed Sci. 51, 702– 707. Rubiales, D., Alca´ ntara, C., Pe´ rez-de-Luque, A., Gil, J., Sillero, J.C., 2003b. Infection of chickpea (Cicer arietinum) by crenate broomrape (Orobanche crenata) as influenced by sowing date and weather conditions. Agronomie 23, 359–362. Rubiales, D., Pe´ rez-de-Luque, A., Cubero, J.I., Sillero, J.C., 2003c. Crenate broomrape (Orobanche crenata) infection in field pea cultivars. Crop Prot. 22, 865–872. Sauerborn, J., 1989. The influence of temperature on germination and attachment of the parasitic weed Orobanche spp. on lentil and sunflower. Angew. Bot. 63, 543–550. Sauerborn, J., 1991. Parasitic Flowering Plants—Ecology and Management. Verlag Josef Margraf, Weikersheim. Sauerborn, J., Linke, K.H., Saxena, M.C., Koch, W., 1989. Solarization: a physical control method for weeds and parasitic plants (Orobanche spp.). Weed Res. 29, 391–397. Stewart, G.R., Press, M.C., 1990. The physiology and biochemistry of parasitic angiosperms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 127–151. Stu¨ tzel, H., Aufhammer, W., 1992. Grain yield in determinate and indeterminate cultivars of Vicia faba with different plant distribution patterns and population densities. J. Agric. Sci. 118, 343–352. ter Borg, S.J., van Ast, A., 1991. Soil moisture root architecture and broomrape (Orobanche crenata) infestation in Faba Bean (Vicia faba). In: Wegmann, K., Musselman, L.J. (Eds.), Progress in Orobanche Research. Universita¨ t Tu¨ bingen, Tu¨ bingen, pp. 278– 292. Turpin, J.E., Robertson, M.J., Haire, C., Bellotti, W., Moore, A.D., Rose, I.A., 2003. Simulating fababean development, growth and yield in Australia. Aust. J. Agric. Res. 54, 39–52. Vega, C.R.C., Andrade, F.H., Sadras, V.O., Uhart, S.A., Valentinuz, O.R., 2001. Seed number as a function of growth. A comparative study in soybean, sunflower and maize. Crop Sci. 41, 748–754.
Effects of environment and sowing date on the competition between faba bean (Vicia faba) and the parasitic weed Orobanche crenata J.H Grenza,*, A.M Manschadib, F.N Uygurc, J Sauerborna a
University of Hohenheim (380), Plant Production and Agroecology in the Tropics and Subtropics, Garbenstrasse 13, 70593 Stuttgart, Germany b Agricultural Production Systems Research Unit, DPI, Toowoomba, Australia c University of Cukurova, Department of Plant Protection, 01330 Adana, Turkey
Received 13 August 2004; received in revised form 2 November 2004; accepted 2 November 2004
Abstract In field trials conducted in southern Turkey during two growing seasons, effects of environment and management on the host–parasite association faba bean (Vicia faba)—Orobanche crenata were quantified. Experimental factors in each experiment included two sowing dates one to two months apart, parasite seedbank densities of 0, 25 and 200 seeds kg1 soil and two susceptible faba bean cultivars. In all treatments, parasitism had minor effects on faba bean vegetative growth. Reductions of stem dry weight occurred in infected crops during grainfilling and were most likely related to increased assimilate retranslocation. Up to 271 parasites m2 attached to the roots of the host, accumulating a maximum biomass of 701 g m2. Parasite number per host was a function of seedbank density and host root length density (RLD) in the top 15 cm of soil. Delayed sowing reduced the combined dry weight accumulation of host and parasite, which was not affected by parasite infection. Pod yield of faba bean ranged from 132 to 1019 g m2 and was affected by pedoclimatic conditions, sowing date and parasite infection. Parasitism mainly decreased host yield by reducing pod number. Seed size decreased to a lesser extent, while seed number per pod was not affected by parasite attack. Timing of host and parasite development phases, namely of the critical phase for faba bean pod setting, strongly affected host–parasite interactions and had decisive influence on the assimilate competition between pods and parasites. Via effects on host and parasite phenology, delayed sowing improved the relative competitive ability of pods during the critical phase, leading to lower parasite number and dry weight. As a consequence, reductions in combined host and parasite dry weight associated with delayed sowing mainly occurred at the expense of parasites. These findings may be transferred into specific control measures aimed at minimising the relative competitive ability of O. crenata during faba bean pod setting. # 2004 Elsevier B.V. All rights reserved. Keywords: Faba bean; Orobanche crenata; Sowing date; Competition; Partitioning; Yield formation
* Corresponding author. Tel.: +49 711 459 3601; fax: +49 711 459 3843. E-mail address: [email protected] (J. Grenz). 0378-4290/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2004.11.001
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1. Introduction Parasitic weeds belonging to the broomrape family (Orobanchaceae) frequently cause massive yield losses to agricultural crops (Parker and Riches, 1993). Central features of broomrape infestation include host specificity, connection to the vascular system of the host plant via a haustorium and a highly persistent soil seedbank (Cubero and Moreno, 1979; Stewart and Press, 1990). One of the most destructive species is Orobanche crenata (crenate broomrape), which inflicts considerable damage upon the production of faba bean (Vicia faba), lentil (Lens culinaris), chickpea (Cicer arietinum), pea (Pisum sativum) and other crops in Mediterranean countries (Sauerborn, 1991). This is all the more detrimental since these food legumes play a major role in providing high value protein in a balanced diet for the people of the affected region. Furthermore, N inputs from biological fixation by legumes are fundamental to sustainable crop production in Mediterranean agricultural systems (Howieson et al., 2000). Much effort has been invested in investigating impacts of O. crenata on host yields, clarifying biochemical aspects of host–parasite interactions and developing control methods (Sauerborn et al., 1989; Foy et al., 1989; Linke, 1992; to cite just a few). Yet none of the tested control measures has proven both effective and economically feasible mainly due to the complexity of host–parasite interactions. An integrated management strategy combining several approaches is most likely to provide durable control of the parasite (Linke and Saxena, 1991a). However, the development of integrated weed management strategies requires quantitative insight into the behaviour of the system under consideration (Kropff and Lotz, 1992). Quantitative information on O. crenata was collected in several studies. Phenological development of the parasite was found to be a function of soil temperature (Arjona-Berral et al., 1987; Sauerborn, 1989). The level of infection mainly depends on parasite seedbank density, degree of host genotype susceptibility to parasitism (Rubiales et al., 2003a) and the host root system (ter Borg and van Ast, 1991; Manschadi et al., 1997). In a field experiment in Syria, Manschadi et al. (2001) demonstrated that O. crenata infecting faba bean mainly grows at the expense of pods that have not yet reached the
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grainfilling phase. They then derived a framework of equations describing growth and development of host and parasite. It is not yet clear whether the described mechanisms are truly generic and can thus be extrapolated to other situations than those studied. Aspects of the interaction, such as N dynamics and the mechanisms causing host-yield reduction, remain unaccounted for. Effects of crop sowing date, specifically the mechanisms involved in the reductions of infection level often found in late-sown host crops (Mesa-Garcı´a and Garcı´a-Torres, 1986; Rubiales et al., 2003b), require further investigation. This study was designed to describe the growth kinetics of the association faba bean—O. crenata as affected by parasite infestation level and crop sowing date under a range of environmental conditions. Objectives were to (i) substantiate existing assumptions about the host–parasite association under different pedoclimatic conditions; (ii) understand the dynamics of assimilate competition between host and parasite and elucidate which growth and development processes are affected and (iii) quantify and explain these processes.
2. Material and methods 2.1. Experimental design Data were collected from on-station trials conducted at the University of Cukurova in Adana (Turkey) in the 2000–2001 and 2001–2002 growing seasons. Experiments were established at two locations per season: Balcali and Yumurtalik in 2000– 2001 and Balcali and Hacihasan in 2001–2002 (Table 1). The experimental station at Balcali is located in the centre of the Cukurova, an alluvial plain in southern Turkey. The parallel trials were situated close to the coast of the Mediterranean. Experiments were set up in a randomised split-split-plot design with four replications, with seedbank levels (SBL) of 0, 25 and 200 viable O. crenata seeds kg1 dry soil as main plot, two faba bean sowing dates per trial as subplot and two faba bean genotypes per trial as sub-subplot (Table 2). Genotypes sown included cultivar ILB 1814 (Syrian Local Large) and the Spanish cultivar Aquadulce, seeds of which were kindly provided by the International Center for Agricultural Research in
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Table 1 Climate and soil characteristics of the experimental locations Location
Coordinates
Rainfalla (mm)
Temperaturea (8C)
Soil type (FAO)
Soil texture
PAWC90b (mm)
pH
Balcali Hacihasan Yumurtalik
37.08N 35.48E 36.68N 35.48E 36.88N 35.88E
648 756 800
18.7 18.8 18.7
Chromic Cambisol Gleyic Cambisol Eutric Cambisol
Loamy clay Silty loam Sandy loam
195 210 149
7.4 8.4 7.7
a b
Long term (25 years) annual sum or average, respectively. Plant-available water capacity to 90 cm depth.
Table 2 Trial years, locations and factor levels in the experiments Trial
Year
Location
Infestation
1 2 3 4
2000–2001 2000–2001 2001–2002 2001–2002
Balcali Yumurtalik Balcali Hacihasan
0, 0, 0, 0,
a
25, 25, 25, 25,
200a 200 200 200
Sowing dates
Cultivars
Dec-1, Jan-4 Dec-2, Jan-6 Nov-5, Dec-13 Nov-8, Jan-26
ILB 1814, Sakiz ILB 1814, Sakiz Aquadulce, Sakiz Aquadulce, Sakiz
Viable O. crenate seeds kg1 soil.
the Dry Areas (ICARDA) at Aleppo (Syria), and the local variety Sakiz. Thousand seed weights (TSW) were 1300, 1150 and 800 g, respectively. None of these genotypes has been reported to display any resistance to O. crenata infection. Faba bean was manually sown at a density of 20 seeds m2 with 50 cm row spacing and 5 cm sowing depth. Prior to sowing, plots were artificially infested with parasite seeds at the desired densities to a depth of 15 cm. No previous Orobanche spp. infestations existed in the fields, thus, controls could be created by leaving parcels noninfested. Parasite seed viability was determined to be 60% by triphenyl–tetrazolium– chloride test (Linke and Saxena, 1991b). The applied total inoculum was therefore 42 and 333 seeds kg1 dry soil, equal to 25.2 and 199.8 mg seeds m2. Broomrape seeds and fertiliser (diammonium-phosphate) were incorporated into the top 15 cm of soil at rates of 20 kg N and 50 kg P2O5 ha1 by use of a rotivator. Insect pests and fungal diseases were controlled chemically (deltamethrin, iprodione), while weeds were removed by repeated hoeing. After the final harvest, crop and parasite residues were burnt and the soil thoroughly harrowed and irrigated. Then the field was solarised by covering it with clear polyethylene sheets during six weeks in July and August to ensure no viable parasite seeds would remain.
2.2. Data collection Air temperature, soil temperature in 10 cm depth, rainfall and global radiation were continuously recorded by weather stations (m-Metos, Pessl Instruments, Austria) installed in the fields. Soil moisture down to 90 cm depth was measured fortnightly in four profiles per location using a time domain reflectometry tube probe system (IMKO, Germany) in the first and the gravimetric method in the second season. The phenological development of host and parasite was recorded weekly. Faba bean phenology was rated using the key of Knott (1990). Sequential biomass harvests as described by Manschadi et al. (2001) were carried out at four-week intervals, starting three weeks after faba bean emergence, to quantify plant organ numbers and dry weights. All broomrapes attached to the sampled faba bean plants were dug out with a spade to 20 cm depth, counted and their dry weight determined. At each biomass harvest, four to six soil monoliths (Bo¨ hm, 1979), 8 cm in diameter and 15 cm high, were taken to 45 cm depth beneath and beside one plant in each noninfested plot. Samples were soaked in water for dispersal and washed over a 1 mm sieve. Roots were scanned, root length measured using the WinRhizoTM program (Re´ gent Instruments, Canada) and root dry weight determined. In the second season, aliquots of all samples were stored in
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airtight bags. Approximately 3 g of each sample were ground in a steel mill and total N content analysed by Dumas dry combustion technique. 2.3. Statistical analysis The concept of thermal time (Ritchie and NeSmith, 1991) was applied to relate events to each other. Thermal time calculations for crop and parasite development from crop sowing and parasite germination to host and parasite emergence, respectively, were based on measured soil temperatures. Base temperatures of 0 8C and 4 8C were assumed for faba bean and O. crenata, respectively (Sauerborn, 1989; Manschadi et al., 2001). Analysis of variance was performed using the General Linear Model procedure of the MiniTabTM (release 13.20, MiniTab Inc.) statistical package. Differences between means were tested for significance by Tukey test (p 0.05). For regression calculations, the SigmaPlotTM (Version 6.00, SPSS Inc.) statistical program was used. For analysis of parasite attachment number, our data were first analysed separately and then pooled with results of Manschadi et al. (2001) to cover a wider range of environmental conditions. Regression analysis had shown the same function types to apply to both data sets. Where genotype differences were nonsignificant, cultivar results were pooled. Parasite numbers and dry weights in trial 4 deviated from the pattern found in the other trials, and parasite development was delayed. Inferring from the similar experience of Manschadi
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et al. (2001), we reasoned that parasite seeds had not been properly incorporated into the soil. Results from infested plots in trial 4 were therefore excluded from analysis. However, weather and soil conditions in this trial resulted in yields of parasite-free plots ranking among the highest ever reported for faba bean. Since data illustrating the potential growth of rainfed faba bean under Mediterranean conditions are rare, results from noninfested plots of trial 4 will be presented here.
3. Results 3.1. Weather conditions In 2000–2001, early-sown crops received 213 mm of rainfall in Balcali and 559 mm in Yumurtalik. In 2001–2002, 756 mm precipitation were measured in Balcali and 812 mm in Hacihasan. Intensive rainfalls in Hacihasan lead to some waterlogging in December 2001, which the crop tolerated well. Temperatures were in the range of the long-term regional average during both growing seasons. Neither frost spells nor excessively high temperatures occurred (Fig. 1). 3.2. Host and parasite phenology Faba beans emerged approximately 300 8C d after sowing, water and cold stress caused some delay. Development from emergence to flowering was accelerated in late-sown crops. The duration of the
Fig. 1. Average monthly temperature (bold line), monthly rainfall (columns) and plant-available soil water from 0 to 90 cm depth (dashed line with symbols) at the experimental locations.
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Table 3 Thermal duration of V. faba and O. crenata development phases in degree-days (8C d) as affected by environmental conditions and sowing date Phase
V. faba sowing– V. faba emergence V. faba emergence– V. faba flowering V. faba flowering– V. faba maturity V. faba emergence– O. crenata emergence
Balcali 2000–2001
Yumurtalik 2000–2001
Balcali 2001–2002
Hacihasan 2001–2002
December 1
December 2
November 5
November 8
January 4
January 6
December 13
January 26
293
266
383
290
416
246
245
235
749
647
738
566
755
743
914
650
1081
945
1216
1152
1577
1406
1453
1122
844
847
764
735
771
784
Figures for V. faba were averaged across genotypes. Thermal time calculations for O. crenata were done using a base temperature of 4 8C.
phase from flowering to physiological maturity displayed the greatest variability and was affected by sowing date and moisture supply. Parasitism caused a shortening of grainfilling by 50–200 8C d, depending on the degree of infection. The period from faba bean emergence, when the first O. crenata seeds can be expected to have been stimulated by root exudates (Linke, 1987), until parasite emergence varied little across trials and treatments (Table 3). 3.3. V. faba stem, leaf and root growth Tiller formation initially progressed at a rate of one additional tiller per 200 8C d, then slowed down, and during grainfilling, stem number was often reduced. Total and per tiller stem weight, but not tiller number, were reduced by delayed sowing in all genotypes. Infection with O. crenata did not affect tiller
formation, but significantly decreased total and per tiller stem weight. Effects of parasitism on stem growth appeared at the start of grainfilling and became significant at mid-grainfilling (Fig. 2). In the most severely infected crop, maximum stem weight was reduced by 46% (trial 3, sowing date 1, Aquadulce) as compared to the control. At physiological maturity, stem N concentration in early-sown crops was 0.8% in noninfected and 0.5% in severely infected faba bean (Fig. 3). Leaf numbers increased at an average rate of one per 32 8C d until grainfilling. Maximum leaf numbers were 50–55 per plant in all three genotypes and were found in early-sown treatments. Parasite infection caused non-significant reductions of leaf number and area (Fig. 4). Leaf N concentration prior to shedding of the last leaves was 3.4% in early-sown noninfected and 2.4% in severely infected faba bean (Fig. 3).
Fig. 2. Course of faba bean stem dry weight under different pedoclimatic conditions as affected by O. crenata infection. Symbol meanings: (*) noninfested control, (&) infested with 25 broomrape seeds kg1 soil, (~) infested with 200 broomrape seeds kg1 soil. E: host emergence; F: flowering; OE: parasite emergence; OM: maturity of infected crops; M: maturity of noninfected crops. Similar courses were obtained from the other locations and sowing dates.
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Fig. 3. Total N concentration in faba bean organs and in O. crenata. Symbol meanings: (*) stem; (& ) green leaf; (~) seed; (^) parasite. Full symbols represent nonparasitised control, hollow symbols treatments infested with 200 viable O. crenata seeds kg1 soil.
Fig. 4. Leaf area index (LAI) of faba bean as affected by sowing date and O. crenata infection (symbol meanings as in Fig. 2).
Faba bean roots were concentrated in the top 15 cm, where mean root length density (RLD) peaked at 2.2–2.3 cm cm3 both beneath and beside plants. RLD was highest in early-sown treatments and crops with good water supply. Root development was more vigorous in 2001–2002 than in 2000–2001. Delayed sowing caused a reduction of maximum RLD in the top 15 cm. 3.4. V. faba shoot growth Growth of faba bean shoots (green, standing, above-ground plant parts) was strongly affected by soil moisture content. The maximum dry weight of noninfected crops sown at Balcali in December 2001 exceeded that of faba bean sown in December 2000 by 23.9%. Shoot dry weight peaked at 488–920 g m2 in
2000–2001, and at 786–1721 g m2 in 2001–2002. Most crops experienced a net loss of shoot biomass from mid-grainfilling until maturity due to leaf senescence and detachment. Trends of shoot N accumulation paralleled those of total shoot growth, with a distinct peak during early grainfilling. Retarded sowing resulted in a shorter growing period, lower growth rates, and consequently less shoot dry weight. Delay by one month reduced the final dry weight of nonparasitised shoots by 10 (trial 3) to 34% (trial 1) (Table 4). In parasitised crops, the biomass reduction caused by delayed sowing mainly occurred at the expense of parasites (Fig. 5). During grainfilling, parasite growth rate often exceeded the combined growth rate of host and parasites, indicating retranslocation from stems and leaves to O. crenata. Parasite infection did not significantly alter combined
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Table 4 Mean values with standard errors () of maximum faba bean shoot dry weight (DW), leaf area index and pod dry weight, as well as O. crenata dry weight and number in crops infested with 0, 25 and 200 O. crenata seeds (OC) kg1 soil, respectively (all weights in g m2) Trial
OC 0
OC 25
OC 200
Sowing date
Faba bean shoot DW
Faba bean LAI
Faba bean pod DW
Faba bean pod DW
Faba bean pod DW
1
1 2
992.9 84.28 645.9 36.03
3.8 0.52 2.1 0.16
495.9 47.89 337.5 15.66
401.2 34.03 285.6 17.54
156.6 26.10 187.1 18.49
2
1 2
1014.0 44.16 742.7 42.85
2.8 0.32 3.2 0.29
637.8 23.68 410.9 29.74
498.6 83.27 383.3 53.89
131.6 30.62 226.3 41.85
3
1 2
1480.7 36.77 1303.4 60.86
4.5 0.21 4.4 0.36
888.8 52.34 869.4 62.95
667.5 77.51 511.9 61.28
165.0 26.44 179.4 34.13
4
1 2
1633.0 80.71 1065.9 48.31
6.0 0.36 5.4 0.32
1019.3 40.55 615.7 35.21
Trial
Sowing date
OC 25, parasite DW
OC 200, parasite DW
OC 25, parasite population
OC 200, parasite population
1
1 2
107.23 20.86 38.43 5.48
265.5 19.00 124.3 11.46
23.8 2.52 14.5 3.52
91.0 9.16 43.3 2.42
2
1 2
114.9 27.27 64.2 9.11
366.4 50.37 171.6 32.31
30.5 6.25 13.0 2.88
115.8 16.84 48.5 12.25
3
1 2
363.5 60.03 214.4 23.15
700.7 66.57 415.6 26.49
77.8 12.55 34.6 5.57
270.6 21.30 151.4 15.13
host and parasite biomass until mid-grainfilling (Fig. 6). Towards maturity, combined host–parasite biomass rapidly decreased in early-sown treatments, leading to lower biomass at harvest as compared to noninfected crops. Parasites accounted for most of the loss by maturing and decomposing earlier than faba bean. At harvest, O. crenata accounted for 50–64% of the combined host–parasite biomass in severely infected
crops. Parasitism also affected amount and composition of harvest residues. Since pods were collected, while parasites remained in the field, total residue weight of infected crops was up to 111% more and residue N up to 72% more than in noninfected faba bean. Severe broomrape infection reduced total N accumulation by up to 52% in 2001–2002. Linear
Fig. 5. Maximum dry weights of faba bean organs and O. crenata at a seedbank density of 200 viable O. crenata seeds kg1 soil as affected by sowing date (black columns: early, grey columns: late; for exact dates see Table 2) under different pedoclimatic conditions.
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Fig. 6. Combined biomass of faba bean and O. crenata as affected by parasite infection under contrasting weather and soil conditions (symbol meanings as in Fig. 2).
regression analysis showed variations in N accumulation to be related to altered assimilate partitioning (r2 = 0.64), not to reduced organ N concentrations (r2 = 0.05). There were no consistent genotype effects on maximum or final values of shoot dry weight or organ N concentrations. 3.5. O. crenata infection and growth Parasite numbers presented here refer to visible O. crenata attachments, both emerged and nonemerged. Parasite numbers varied from 13 to 271 m2, equalling 0.7–13.6 per host plant. Increased shoot dry weight caused by better moisture supply, as in trial 3, resulted in higher parasite numbers and dry weight (Table 4). Delaying sowing by one month reduced parasite numbers in plots infested with 200 viable parasite seeds kg1 soil by 52, 58 and 44% in trials 1, 2 and 3, respectively. Results of Manschadi et al. (2001), who collected data from faba bean cultivar ILB 1814 grown at infestation levels of 50, 200 and 600 viable O. crenata seeds kg1 soil in northwest Syria, were included in the following analysis to expand the range of conditions. Response functions of parasite number to the variables considered were similar in our experiments and those of Manschadi et al. (2001). Attachment number mainly was a function of parasite seedbank level and maximum host RLD in 0–15 cm depth. Parasite numbers increased up to a RLD of slightly above 2.0 cm cm3. Since effects of RLD ceased beyond that level, regression analysis of parasite number as affected by SBL was only
performed for treatments where RLD exceeded 2.1 cm cm3. A rectangular hyperbolic function yielded the best fit (Fig. 7, left). Effects of RLD on attachment number were analysed for treatments with SBL of 200 seeds kg1 soil, since this level was included in all trials. The best fit was achieved by a sigmoidal function (Fig. 7, right). Assuming no mutual interactions between SBL and RLD, the hyperbola was linearly transformed and multiplicatively coupled with the sigmoidal function. Linear regression of calculated against observed parasite numbers showed the resulting two-factorial equation P ¼ 307:1=ð1þ eððRLD-1:49Þ=0:41Þ Þð3:8 SBL=ð552:46 þ SBLÞÞ
where P (parasites m2) is a function of RLD (cm cm3) and SBL (viable seeds kg1 soil, 0–15 cm depth), to explain 95% of the observed variation in maximum parasite number. In severely infected crops, final parasite number was less than 50% of the maximum, since many attachments died before emergence. Parasite growth was rapid, average daily growth rates during faba bean grainfilling reached up to 1.17 g m2 8C d1, equaling 230 kg ha1 d1. Maximum O. crenata dry weight was 366 g m2 in 2000– 2001 and 701 g m2 in 2001–2002 (Table 4). Average individual parasite dry weight was negatively correlated with attachment number, but was not affected by sowing date or cultivar. Total N concentration in O. crenata tissue was close to 2% across trials, treatments and development stages (Fig. 3).
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Fig. 7. Maximum O. crenata attachment number as affected by parasite seedbank density in treatments with maximum faba bean root length density above 2.1 cm cm3 (left) and as affected by maximum faba bean root length density at a seedbank density of 200 viable O. crenata seeds kg1 soil (right). Symbol meanings: (*) experiments described in Table 2; (~) experiments of Manschadi et al. (2001).
3.6. V. faba yield formation Faba bean pod dry weight at harvest ranged from 132 to 1019 g m2 (Table 4), seed dry weights varied between 101 and 831 g m2. Seeds accounted for 80% and husks for 20% of pod weight, with no significant variations across trials and treatments. All findings on pod yield presented here similarly apply to seed yield. Pod and seed yield were significantly affected by all experimental factors. When sowing was delayed by one month, the pod yield of noninfected faba bean decreased by 32, 36 and 2% in trials 1, 2 and 3, respectively. In parasitised plants, pod growth was slowed down, while combined pod and parasite dry weight increased at the same rate as in noninfected crops. Parasitism on average reduced pod yield by 25 and 71% at infestation rates of 25 and 200 viable parasite seeds kg1 soil. The response curve of pod yield to the number of O. crenata attachments followed a hyperbolic decay function (Fig. 8). Delayed sowing diminished crop yield loss caused by O. crenata. In parcels infested with 200 viable parasite seeds kg1 soil, average yield loss due to parasitism was 81.4, 72.3 and 45.9% in crops sown in November (trial 3, sowing date 1), December (trials 1 and 2, sowing date 1; trial 3, sowing date 2) and January (trials 1 and 2, sowing date 2), respectively. Pearson correlations between pod yield and factors of yield formation were +0.299 for TSW, +0.247 for the number of seeds per pod, and +0.884 for pod number per m2. Linear regression showed pod number
Fig. 8. Relative faba bean pod yield, calculated as fraction of the yield measured in the respective noninfected control, as affected by O. crenata attachment number. Symbol meanings: (*) trial 1; (^) trial 2; (& )trial 3 (see Table 2).
to explain 74.7, 76.6 and 80.4% (r2) of observed variations in pod yield in trials 1, 2 and 3, respectively. The respective figure for the combined data sets was 73.6% (Fig. 9). Adding seeds per pod and TSW to the regression equation increased r2 to 88.5, 93.1 and 97.4%, respectively. Pod number was significantly reduced by delayed sowing and by parasitism. The effect of O. crenata infection set on at podsetting and was significant across locations, sowing dates and cultivars. Seed number per pod significantly differed between genotypes and responded negatively to delayed sowing, but not to parasitism. Delayed sowing resulted
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Reductions of total seed N in infected crops reached 89% and were mainly related to reduced seed dry weight (r2 = 0.95), not to lower seed N concentration. See Table 5 for a comprehensive summary of consistent effects of experimental factors on faba bean and O. crenata growth and development.
4. Discussion 4.1. Determinants of O. crenata infection
Fig. 9. Effect of pod number on pod yield: relative faba bean pod yield, with the yield of nonparasitised treatments set 1.0, as affected by relative pod number (symbol meanings as in Fig. 8).
in significantly reduced TSW in the control treatments. Infestation with 200 parasite seeds kg1 soil caused reductions of TSW by 30.8, 27.7 and 20.9% in early-sown, and by 6.3 (increase), 22.2 and 21.4% in late-sown treatments of trials 1, 2 and 3, respectively. There was a significant interaction between effects of delayed sowing and parasitism on TSW. Severe parasite attack reduced final seed N concentration of early-sown faba bean from 4.2 to 3.7% (Fig. 3).
The extent of O. crenata effects on host growth is a function of parasite number and assimilate demand per parasite (Manschadi et al., 2001). The main determinant of parasite number at given SBL was maximum RLD, which is in accordance with previous findings (ter Borg and van Ast, 1991; Manschadi et al., 2001). The response of parasite number to RLD followed a sigmoidal curve approaching an asymptote at RLD of 2.0–2.5 cm cm3. Parasite stimulation depends on the presence of a host root less than 2 mm from the seed (Linke and Vogt, 1987), hence it is plausible that the number of stimulated broomrape seeds rises with increasing RLD. The asymptote marking complete stimulation of the seedbank was lower at high values of SBL, most likely due to
Table 5 (a) Effects of parasite infestation, sowing date and genotype consistent (p 0.05, General Linear Model) across trials 1, 2 and 3 Parasite infestation
Sowing date
Genotype
Postflowering development (+) Maximum crop standing DW () Stem DW at harvest () Pod No at harvest () Pod DW at harvest () Maximum parasite No (+) Maximum parasite DW (+) Mean DW per parasite ()
Preflowering development (+) Postflowering development (+) Maximum crop standing DW () Maximum system DW () (=crop + parasite) Stem DW at harvest () Maximum parasite No () Maximum parasite DW ()
Stem DW at harvest (Sakiz < ILB1814/Aquadulce) Mean seed DW at harvest (Sakiz < ILB1814/Aquadulce) Mean seed No per pod (Sakiz > ILB1814/Aquadulce)
(b) Variables consistently not affected by parasite infestation, sowing date or genotype (p 0.05, General Linear Model) across trials 1, 2 and 3 Preflowering development Maximum stem No Maximum crop standing DW Maximum system DW Pod No at harvest Maximum system DW Maximum stem No Mean seed No per pod Maximum stem No Maximum leaf/node No Maximum leaf No Maximum leaf DW Maximum leaf DW Mean seed No per pod Maximum parasite No Maximum parasite DW Mean DW per parasite Symbol meanings: (+): increased growth/accelerated development at higher infestation level/delayed sowing; (): reduced growth or slower development; (DW): dry weight; (No): number.
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intraspecific competition. The response of attachment number to SBL followed a hyperbola nearly linear at low, but asymptotic at high levels of infestation. This asymptotic curve is typical for density-dependent functions (Naylor, 2002) and reflects intraspecific competition. This may also explain why many parasites did not emerge when population density was high. Furthermore, average parasite dry weight was lower in severely infected crops. Other factors that can affect attachment number, such as fatal germination due to low soil temperature (Sauerborn, 1989) and resistance mechanisms leading to reduced establishment of attachments (Rubiales et al., 2003a), did not seem to play a role in our experiments. Our results suggest that at the given sowing density, one plant of faba bean cultivar ILB 1814 or Aquadulce growing under near-optimal conditions can support either about 10 well-developed pods or 10 to 15 full-grown O. crenata individuals until physiological maturity. This carrying capacity of the crop is a function of biomass accumulation, which in turn depends on pedoclimatic conditions and sowing date. 4.2. Effects of parasitism on V. faba Within the range of conditions encountered, O. crenata infection had no effects on the vegetative growth phase of faba bean, which is in accordance with findings of Mesa-Garcı´a and Garcı´a-Torres (1984). Parasitism had minor influence on size and functionality of the host leaf apparatus, thus on assimilative capacity. Accordingly, the combined growth of host and parasite did not differ from that of noninfected crops, as also observed by Manschadi et al. (1996). The only significant effect of parasitism on vegetative growth was a reduction of stem biomass during grainfilling. This indicates increased retranslocation of assimilate to parasites, which explains how parasites could grow at faster rates than host and parasites combined. Effects of parasitism on host N metabolism were weak. Minor reductions of N concentration affected stems, leaves and seeds during grainfilling. Replacement of pods containing 4% N by parasites with only 2% N resulted in lower system N accumulation. Contrary to findings of el-Ghamrawy and Neumann (1991), extremely reduced N concentrations did not affect any plant organ. Reduced N
uptake of infected crops was related to altered carbohydrate partitioning and testifies a dominance of C over N flows. While O. crenata did not disturb assimilate production, it massively altered the sink side of the assimilate balance. Biomass loss in the host mostly occurred at the cost of pods, which are the organs with which parasites mainly compete for assimilate (Manschadi et al., 1996). Yield of grain legumes is the product of pod number, seed number per pod and TSW (Egli, 1998). In faba bean, pod number is the major determinant of yield variations (e.g. Pilbeam et al., 1989; Adisarwanto and Knight, 1997; Loss and Siddique, 1997). Pod and seed number are a function of crop physiological status during a critical period (Jiang and Egli, 1995; Egli, 1998; Vega et al., 2001). In faba bean, this period begins around the start of flowering and lasts approximately 550 8C d (Stu¨ tzel and Aufhammer, 1992). Sink strength of legume pods during most of the critical period is proportional to organ biomass (Jeuffroy and Devienne, 1995, on pea). During this phase, reduced assimilate supply due to insufficient sink strength results in pod abortion (Egli and Bruening, 2001, on soybean (Glycine max)). During the subsequent grainfilling phase, when sink strength is at its maximum, pod and seed numbers are no longer subject to change (Egli, 1998). The time course of sink strength and biomass accumulation follows a sigmoidal pattern consisting of lag, linear and maturation phase in legume seeds and pods (Egli, 1998), as well as in O. crenata individuals (Manschadi et al., 2001). Parasitism reduced pod number and caused some reduction of TSW. Since pod number in parasitised crops was reduced from pod setting onwards, we can assume that pods and parasites started to compete for assimilate during the critical period. By developing faster and entering the linear growth phase earlier than pods, parasites accumulated sufficient sink strength to outcompete pods, which were aborted. Hence, the competitive abilities of pods and parasites during the critical period decided about their fate. Parasites then benefited from the inherent stability of the legume sink hierarchy. TSW results from rate and duration of seed growth. Its reduction was probably caused by a shortened grainfilling duration due to accelerated senescence.
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Lower faba bean TSW associated with shortened grainfilling was also reported by Loss and Siddique (1997) and Loss et al. (1997). Reduced seed growth rate is unlikely to have played a role, since it was shown by Munier-Joulain et al. (1998, on pea, lupin (Lupinus albus) and soybean) that even strongly reduced assimilate availability during grainfilling did not affect growth rates of legume seeds. The responsiveness of host–parasite interactions to shifted sowing date testifies the importance of the timing of host and parasite development stages, as reckoned by Manschadi et al. (1996). The biochemical adaptions that enable parasites to seize the place of pods as sinks for assimilate, with their distance from the source tissues obviously not imposing a problem, remain to be elucidated. Phytohormones are likely to play a role, since substances from the cytokinin group are important in the regulation of fruit production and abortion of legumes (Nagel et al., 2001; Liu and Longnecker, 2002). El-Ghamrawy and Neumann (1991) found applications of kinetin to the host apex to increase pod number in faba bean infected with O. crenata. Specific control measures should aim at minimising the competitive ability of parasites relative to that of pods during the critical period of legume pod setting. Assimilate allocation to pods can be stimulated by phytohormone applications (el-Ghamrawy and Neumann, 1991). Improving the timing of sowing, fertilisation and irrigation measures could help synchronise assimilate supply with the critical period of pods, but desynchronise it with the maximum demand of parasites. Alternatively, it might be possible to retard or disturb development and growth
311
of parasites during the critical phase by herbicide application (Foy et al., 1989). Information on the likely occurrence of the critical period, which could be generated by simulation models, might help optimise the timing of such measures. 4.3. Effects of sowing date on host–parasite competition Delayed sowing resulted in reduced faba bean growth and yield, the latter of which was mainly associated with lower TSW. Late-sown crops are subjected to the senescence-accelerating heat and water stress of the Mediterranean summer at an earlier stage, which leads to a shorter grainfilling period. Correlations between shorter grainfilling phase and reduced TSW were also observed by Adisarwanto and Knight (1997) and Loss et al. (1997). The negative effect of delayed sowing on the level of O. crenata infection observed in previous studies (Mesa-Garcı´a and Garcı´a-Torres, 1986; Manschadi et al., 2001) was confirmed. Similar responses to delayed sowing were reported for O. crenata infecting carrot (Daucus carota) (Eizenberg et al., 2001), chickpea (Rubiales et al., 2003b) and pea (Rubiales et al., 2003c). Reduced parasite numbers and biomass in late-sown crops have mainly been attributed to effects of soil temperature on parasite development. Suboptimal temperatures are likely to cause a high percentage of fatal germination and a delay in parasite development (Sauerborn, 1989), while in crops sown in autumn, parasites may establish before the onset of cold temperatures (Rubiales et al., 2003b) and benefit
Fig. 10. Schematic representation of the effect of sowing date on phenological development of faba bean and O. crenata (S: sowing; E: emergence; F: flowering; P: pod setting; M: maturity; G: germination). The line in the background represents daylength. Arrows indicate the approximate start of pod and parasite linear growth, respectively. In late-sown crops, the competitive advantage of parasites is neutralised.
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from a head start relative to generative organs of the host in spring. Other factors that may affect host– parasite interactions include moisture supply, host RLD and photoperiod. In late-sown crops, development phases are shifted towards summer, when water supply becomes limiting. However, direct effects of moisture supply on parasite growth and development were not found. The observed reduction of parasite number in late-sown faba bean indeed went along with lower RLD, which may have resulted in a lower probability of parasite seed stimulation. However, the irrigated trials of Manschadi et al. (2001) showed that delayed sowing not always leads to reduced root growth, hence this mechanism is probably not generic. Photoperiod has major effects on crop phenology. Faba bean is a quantitative long-day plant responding to daylength during most pre- and postflowering development phases (Turpin et al., 2003). In the Mediterranean region, crops sown in autumn enter the photoperiod-sensitive phase of development when daylength is at its annual minimum. Delayed sowing corresponds with a shift to periods of longer days, leading to accelerated development. The development rate of O. crenata on the contrary is solely driven by ambient temperature (Manschadi et al., 2001). Late-sown faba bean reached flowering, hence the critical period, within less thermal time, while the duration of parasite development was constant across sowing dates and environments. Effects of drought stress accelerating faba bean development may have added to this difference. Faster development may allow late-sown faba bean to enter the phase of linear seed growth earlier and thus have higher sink strength than parasites during the critical period. Delayed sowing thus reduces or neutralises the head start in the competition for assimilate during the critical phase that parasites have in early-sown crops (Fig. 10). Consequently, relatively less pods and more parasites are aborted. Parasites are obviously unable to compensate for this advantage of the crop, neither by transmitting some biochemical signal nor by accelerating their own development.
Acknowledgement This work was financially supported by a scholarship of the German National Academic Foundation.
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