Prevention of pea lodging by intercropping barley with peas at different nitrogen fertilization levels

Field Crops Research 149 (2013) 95–104

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Prevention of pea lodging by intercropping barley with peas at different nitrogen fertilization levels Magdalena Podgórska-Lesiak, Piotr Sobkowicz ∗ Department of Agroecosystems and Green Areas Management, Wrocław University of Environmental and Life Sciences, pl. Grunwaldzki 24a, 50-363 Wrocław, Poland

a r t i c l e

i n f o

Article history: Received 5 September 2012 Received in revised form 24 April 2013 Accepted 25 April 2013 Keywords: Barley–pea intercrop Facilitation Competition Plant lodging LER

a b s t r a c t Field pea (Pisum sativum L.) that is grown in pure stands tends to lodge, which may lead to decreased grain yields. Barley (Hordeum vulgare L.) intercropped with peas prevents lodging, but this facilitative effect of the cereal on the pea has rarely been examined. Two two-factorial experiments (Experiment 1 and Experiment 2) were conducted in 2005, 2006, and 2007 to study interactions between barley and a medium-tall, leafy field pea (Wiato cultivar) and between barley and a tall, leafy field pea (Fidelia cultivar). In both experiments, mineral N fertilizer was used at rates of 0, 30, and 60 kg of N ha−1 . Experiment 1 was conducted to evaluate plant lodging, grain yield, the intercrop yield advantage over pure stands and competition between the intercropped species. Experiment 2 was designed to separate the facilitative effect of the mechanical support provided to the peas by the barley in the intercrop from the effects of competition. In the experiment, groups of four pea plants were grown supported by an iron wire frame to prevent their lodging. The frames were kept in the plots until the peas flowered fully or reached full maturity. Similar groups of legumes were also grown in mixtures with nine barley plants. These treatments permitted the determination of the net benefits to the peas of the mechanical support provided by the added barley between pea flowering and maturity. In Experiment 1, there was little lodging of the pea cultivars in the intercrops, whereas the pure stands lodged severely. In all years, the barley–pea intercrops were more productive than the sole crops (LER > 1). The barley–Wiato mixture yielded more grain than the barley–Fidelia mixture in 2005 and 2006. Both mixtures transgressively overyielded in 2006 at the nitrogen fertilizer rate of 30 kg of N ha−1 , and the barley–Wiato mixture did so at 0 kg of N ha−1 . Experiment 2 showed that mechanical plant support (facilitation) was more important for the tall cultivar Fidelia than for the medium-tall cultivar Wiato, but Fidelia was the weaker competitor of the two with barley. Increasing the N fertilizer rates decreased the pea tolerance to competition from barley in the intercrop. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Mixed cropping has been widely practiced in the traditional agriculture of developing countries because it is considered more efficient than sole cropping and because it reduces the risk to farmers (Altieri, 1999; Vandermeer, 1989; Zhang and Li, 2003). Legume–nonlegume intercrops have gained attention in developed countries, mainly in terms of the crop rotations of organic farming systems in which legumes play an important role as a source of N (Bulson et al., 1997; Hauggaard-Nielsen et al., 2009; Schmidtke et al., 2004). The primary and most frequently reported type of interaction in such cropping systems is competition. It is particularly intense in the intercrops grown for yield maximization per unit

∗ Corresponding author. Tel.: +48 71 320 1670; fax: +48 71 320 1683. E-mail address: [email protected] (P. Sobkowicz). 0378-4290/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fcr.2013.04.023

area (Sobkowicz and Tendziagolska, 2005). In the barley–pea intercrop, the barley is often observed to be dominant. This dominance is attributed to the faster initial growth of the cereal and its high competitive uptake of soil N (Andersen et al., 2004; Corre-Hellou et al., 2006, 2007; Hauggaard-Nielsen et al., 2001a,b, 2009; Jensen, 1996a). Other authors found that the competitive ability of pea plants depends on their height. Tall pea cultivars are better able to compete with cereals than shorter ones (Hauggaard-Nielsen and Jensen, 2001; Rauber et al., 2001). Research also showed that the conventional leafy cultivars are better competitors than the semileafless ones (Rauber et al., 2001; Semere and Froud-Williams, 2001; Tofinga et al., 1993). The competitive abilities of the components of the intercrop are influenced by nitrogen fertilizer inputs. In research with cereal–pea intercrops, increased N fertilizer increased the competitive ability of the cereal (Andersen et al., 2004; Chen et al., 2004; CorreHellou et al., 2006; Hauggaard-Nielsen and Jensen, 2001; Jensen, 1996a).

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The yield advantage of intercrops is attributed mostly to resource complementarity, which is an emergent property that occurs in mixtures of populations and stems from differences in resource acquisition by the component species. The mixture utilizes the limiting resource or resources more completely than the pure stands (Bulson et al., 1997). In legume–nonlegume mixtures, the two components use partially different nitrogen sources, and when the nutrient is limited, indices that assess intercrop production demonstrate the advantage of such intercrops over pure stands. This relationship was shown in experiments using different N fertilizer inputs (Andersen et al., 2004; Chen et al., 2004; CorreHellou et al., 2006; Hauggaard-Nielsen and Jensen, 2001; Jensen, 1996a). Several authors have noted that the intercrop advantage may also result from interspecific facilitation, the positive influence of plants of one species on plants of another species (HauggaardNielsen and Jensen, 2005; Vandermeer, 1989). Facilitation and competition have been extensively studied by plant ecologists who emphasize that because both interactions operate in plant communities, the results of many experiments show only the net outcome of the two phenomena (Bruno et al., 2003; Callaway, 1995; Callaway and Walker, 1997; Holmgren et al., 1997). In the cereal–legume intercrop, the direct transfer of fixed N from the legume roots to the cereal roots is an example of facilitation (Brooker et al., 2008). Although the process has not been adequately demonstrated under field conditions (Cochran and Schlentner, 1995; Hauggaard-Nielsen and Jensen, 2005; Jensen, 1996a), fixed N can be released from the mineralizing roots of the legume plant and taken up by cereal plant roots (Jensen, 1996b; Stern, 1993). Hauggaard-Nielsen and Jensen (2005) and Zhang and Li (2003) reviewed several other underground facilitation mechanisms existing in intercrops and indicated that these mechanisms should be taken into consideration when assessing intercrop efficiency. Callaway (1995) demonstrated a facilitation mechanism in which some plant species use the stems of other species as mechanical support for their growth. This situation is similar to that observed in cereal–legume intercrops in which the second component is a climbing plant, such as pea or vetch, which needs support for its successful growth. The legumes attach to the stiff culms of the cereal by tendrils. In this way, the cereal facilitates the growth of the legume, but the weight of the legume interferes directly with the growth of the cereal. This mechanism allows the legume to gain access to light and possibly to more effectively compete for the resource. Because it is taller than barley, Iptas (2002) found that triticale instead of barley intercropped with Hungarian vetch resulted in higher vetch growth and yields. Although this type of facilitative interaction is directly visible in the legume–nonlegume intercrop, it may be recognized as facilitation in agronomic terms only when the facilitated species yields more because of such support than when it grows unsupported. In other words, the interspecific facilitation has to be greater than the intraspecific facilitation that exists in the pure legume stand. Research clearly documents that the susceptibility of pea to lodging results in decreased yields. Annicchiarico and Iannucci (2008) found a negative correlation between susceptibility to lodging and grain yield among 37 pea cultivars. Schouls and Langelaan (1994) suggested that the main reasons for grain yield losses in pea were the worsened light penetration into a lodged canopy and the lack of assimilates for later-forming pods. A decrease in the grain yield of pea resulting from lodging was also demonstrated by Wang et al. (2006) in an experiment in which one treatment artificially prevented lodging of the pea canopy. Other research showed that leafy pea cultivars were more prone to lodging than semileafless ones (Annicchiarico and Iannucci, 2008; Schouls and Langelaan, 1994; Uzun and Ac¸ıkgöz, 1998; Uzun et al., 2005; Wang et al., 2006). According to Uzun et al. (2005), tall pea cultivars lodged more than

shorter ones. Consequently, lodging has biological meaning being inherent in the growth of pea. Thus, when the legume is grown in mixed stands with cereal, aboveground facilitation operates in the intercrop. In intercropping experiments with pea, plant lodging has rarely been examined. Corre-Hellou et al. (2011) attributed the greater weed infestation of pure pea stands than barley–pea mixtures to lodging of the legume. Kontturi et al. (2011) observed severe lodging of certain semileafless pea cultivars in pure stands and demonstrated that even small numbers of oat plants effectively reduced lodging in an oat–pea intercrop. Rauber et al. (2001) found a high-yield advantage when intercropping oats with conventional tall, leafy pea cultivars and suggested that the advantage occurred because the cereal prevented lodging of the pea. The importance of this type of facilitation has also been shown in research with other crops. Revilla-Molina et al. (2009) questioned the role of resource complementarity in a varietal rice mixture. They demonstrated that the yield advantage of the mixture over the pure stands resulted from the support that one cultivar provided to another. Based on the available studies, it may be assumed that the aboveground facilitation of pea by barley is yet another interaction apart from competition that exists in the intercrop mixture. Observation of the canopy of such an intercrop, where the attachment of the pea tendrils to the barley allows the legume to climb to the top of the canopy and gain more light, suggests that the phenomenon may positively affect pea yields. The aims of the present research were to determine the grain production of intercrops of barley with two cultivars of field pea and to analyze the interactions between the component species at different levels of N fertilization. For the purpose of this study, two experiments were conducted: a field experiment (Experiment 1) and a microplot experiment (Experiment 2). The field experiment was designed to evaluate the effects of N fertilizer input on plant lodging, grain yield, the intercrop yield advantage and interspecific competition. The microplot experiment was designed to assess the importance of the supportive function of barley against pea lodging, which is understood to be a facilitative interaction, and the role of N fertilizer input in modifying this facilitative interaction and in interspecific competition. 2. Materials and methods A pair of two-factorial experiments was conducted in 2005–2007 in Wrocław at the Swojec Agricultural Experimental Station of Wrocław University of Environmental and Life Sciences. Both experiments were conducted in the same field on alluvial loamy sand soil of 5.5–5.6 pH containing 0.5 g kg−1 of total N in the 0–20 cm layer. Oats was the preceding crop before both experiments each year. After harvesting the oats and collecting the straw, the soil was tilled shallowly. Before winter, the field was plowed to a depth of 25–27 cm. In spring, the field was harrowed with a spike-tooth harrow and fertilized each year with triple superphosphate and potassium chloride at a rate of 22 kg of P ha−1 and 66 kg of K ha−1 . 2.1. Weather conditions The weather conditions varied during the experimental period (Fig. 1). The rainfall was highly variable during the 2005 growing season. In May, the rainfall was more than two times the 37-year average, whereas June precipitation approached only half of the monthly long-term average. A prolonged period of snow cover in March 2006 due to low air temperatures caused a two-week delay in sowing the experiments. Adverse water conditions in May and July 2006 together with a high air temperature in July accelerated

M. Podgórska-Lesiak, P. Sobkowicz / Field Crops Research 149 (2013) 95–104

rainfall temperature

25 20

150

15 100 10 50

Temperature (oC)

Rainfall (mm)

200

5

0

0 MAM J J A

MAM J J A

MAM J J A

MAM J J A

2005

2006

2007

1968-2004

Fig. 1. Monthly mean air temperatures and rainfall sums from March until August during the experimental years and averaged over the period of 1968–2004. Data collected from the Agro- and Hydrometeorology Observatory in Swojec, Wrocław.

crop maturation. In 2007, rainfall was more evenly distributed than in 2005 and 2006. Extremely low rainfall in April 2007 did not interfere with plant emergence and the early growth of plants because of a sufficient amount of water collected in the soil in March. 2.2. Experiment 1 2.2.1. Experimental design In Experiment 1, spring barley (Hordeum vulgare L.) cultivar Refren, the Wiato and Fidelia field pea (Pisum sativum L.) cultivars and mixtures of barley with each pea cultivar were grown at three levels of nitrogen fertilization: 0, 30 and 60 kg of N ha−1 . The experiment was a randomized split-plot design with the N levels as the main plots and the pure stands and intercrops as the subplots. Four replicates were used for each factor. The medium tall, leafy Wiato is the cultivar destined for dry seed, whereas the tall, leafy Fidelia is the green fodder/dry seed cultivar. The recommended seeding densities were used for the pure stands of both crops: 330 and 90 viable seeds m−2 for barley and pea, respectively. The crop mixtures were prepared according to the proportional substitutive design (Jolliffe, 2000), with a seeding density of 30% (99 seeds m−2 ) that of the barley sole crop and 70% (63 seeds m−2 ) that of the pea sole crop. This relative dominance of the pea seed in the seeded mixture was planned because of the expected lower competitiveness of the legume species. 2.2.2. Field management The experimental area was harrowed with a spike-tooth harrow before sowing. The experiment was sown on April 6, 2005; April 18, 2006; and April 3, 2007. Separate, parallel passes of a seeder were used to sow the mixture components. The pea seeds were sown first to a depth of 6–7 cm, and then, the barley seeds were sown to a depth of 3–4 cm. The row spacing for each species was 12.5 cm in both the pure and mixed stands. The area of each plot was 16.25 m2 (1.25 m × 13.0 m). The nitrogen fertilizer was applied by hand immediately after sowing as urea with 46% N according to the experimental design. Weeds were controlled with Basagran 600 SL (BASF SE Ludwigshafen, Germany) (bentazon) (2 l ha−1 ) and the adjuvant Atpolan 80 EC (Zakład Produkcyjno-Handlowy “Agromix”, Niepołomice, Poland) (paraffin oil) (1.5 l ha−1 ) applied to the experimental area on May 19, 2005; May 26, 2006; and May 18, 2007. Fastac 100 EC (BASF Agro B.V., Arnhem, Netherlands) (alpha-cypermethrin) (0.15 l ha−1 ) was used against aphids on June 28, 2005. The plots were harvested with a plot combine harvester after both species reached full maturity on August 20, 2005; August 3, 2006; and August 12, 2007.

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2.2.3. Measurements and analyses At full maturity of the crops, plant lodging was assessed visually on each plot using the following method of Stapper and Fischer (1990): ls =

pײ , 90

where ls is the lodging score, p is the percentage of the plot area that lodged, and ˛ is the angle of deviation of the plant stems from the vertical. This equation provides a lodging score range from 0 (crop not lodged) to 100 (crop completely lodged). In the mixtures, lodging was assessed separately for each crop. Only the lodging data for peas are presented here. After the lodging assessment, plant samples were collected from the plots by digging up four neighboring rows 1 m long (0.5 m2 ) of each species in the pure and mixed stands. The ears were threshed in a sample thresher; the pods were shelled by hand. After weighing the grain, the percentage of each species in the mixed yields was determined and used to calculate the individual yields of each species in the grain yield of mixtures harvested from the plots using the combine harvester. The advantage of the mixed over the pure stands was determined by comparing the absolute yields of the mixtures with those of the pure stands and by using the land equivalent ratio (LER) (Mead and Willey, 1980). This ratio shows the total land area of crops grown alone that provides the same production as a unit of land growing a mixture of these crops as follows: LER = RYb + RYp ,

RYb =

Ybp Ybb

,

and RYp =

Ypb Ypp

,

where RYb is the relative grain yield of barley, RYp is relative grain yield of pea, Ybp is the grain yield of barley in mixture with pea, Ybb is the grain yield of pure-stand barley, Ypb is the grain yield of pea in mixture with barley, and Ypp is the grain yield of pure-stand pea. To compare the relative competitive ability of barley in relation to pea, the competitive balance index (Cb ) was used (Wilson, 1988). This index is the natural logarithm of the competitive ratio (CR) (Weigelt and Jolliffe, 2003; Willey and Rao, 1980) and is given by the following equation:



Cb = ln CR = ln

RYb RYp



pp pb



,

where pp is the proportion of pea in seeded mixture (0.7), and pb is the proportion of barley in seeded mixture (0.3). In the present experiment, Cb > 0 indicates that barley was a better competitor than pea. 2.2.4. Statistics An analysis of variance for split-plot experiments was performed on data from each year according to Gomez and Gomez (1984), considering nitrogen levels as the main-plot factor and crops as the subplot factor and calculating the interaction between these factors. When the F value was significant, the treatment means were compared with the least significant difference test (LSD) at P = 0.05. Each analysis of variance was performed with four replicates on untransformed data, with one exception. The lodging score data for the pea cultivars were square root (x + 0.5) transformed before the analysis because of large differences among the treatment means and the presence of data points with a value of zero. 2.3. Experiment 2 2.3.1. Experimental design and planting pattern Experiment 2 used plots of 1 m2 area (1 m × 1 m) and the same species and cultivars as those grown in Experiment 1. A randomized

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split-plot design included nitrogen fertilization levels of 0, 30, and 60 kg of N ha−1 as the main plots. The second factor measured the response of the pea cultivars to the aboveground facilitation and competition from barley. Each pea cultivar was represented by four plants per plot. The pea plants were grown (a) in pure stands surrounded by iron wire frames that prevented them from lodging until the full flowering stage, (b) in pure stands surrounded by the frames that prevented them from lodging until full maturity, and (c) in mixtures with nine barley plants. Four replicates were used for each factor. The pea plants were grown at each corner of a 10 cm× 10 cm square centered in the middle of each plot. In the mixture, the nine barley plants were grown in a 3- × 3-plant arrangement 10 cm from each other in a square pattern that intermingled regularly with the four pea plants. In this way, each pea plant was in the center of a square formed by four barley plants. Thus, a partial additive design was used to form the experimental crop mixture, with the same number of pea plants in the pure stands as in the mixture with barley (Gibson et al., 1999). This design allowed the separation of the detrimental and beneficial influences of the barley on the peas. Before sowing, the soil was raked to a smooth surface. To attain the planting arrangement, the barley and pea seeds were sown by hand to a depth of 4 and 6 cm, respectively, using a perforated plywood sheet and two seeds per hole. Sowing was performed on April 7, 2005; April 21, 2006; and April 6, 2007 and followed the next day by the hand application of 46% N urea to each plot according to the experimental design and the mixing of the urea into the soil with a rake. After plant emergence, the plants were thinned. The supporting frames were constructed from 3.5 mm iron wire painted medium green. The frames were 80 cm high and had three regularly spaced 20 cm diameter rings that were positioned horizontally. The rings were connected by three straight wires that extended beyond the frame ends and were pressed into the soil to a depth of 15 cm. The frames were mounted on all pure-stand pea plots a few days after plant emergence, with the rings surrounding the area containing the pea plants. When left until the peas were fully mature, the purpose of the frames was to simulate the supporting function of intercropped barley plants in preventing pea lodging. When left until the peas reached the full flowering stage, the frames simulated the self support of pea plants grown in pure stands, as observed in the plots of Experiment 1. The frames were removed from the plots at the stage when the peas in the pure stands began to lodge in Experiment 1. The two treatments made it possible to determine the net facilitative (plant supporting) effect of the barley on the pea in the mixture. It was assumed that the frame had no negative influence on the peas. The experiment was regularly weeded by hand during the growing season. 2.3.2. Measurements and analyses At full maturity, all the pea plants were cut at the soil surface in each plot, the pods were removed from the plants, and all the plant material was dried at 70 ◦ C to constant weight. After drying, the pods, straw and seeds were weighed. The dry weight of the seeds and of the biomass was calculated on a per plant basis. It is assumed that barley competes with pea for resources belowand aboveground, but aboveground, it also facilitates pea growth by providing support for the climbing legume. Pea is therefore positively affected by receiving support from barley and negatively affected by competition with barley. Thus, the total influence of barley on pea is the sum of the two interactions. To assess the positive and negative effects of the barley on the pea cultivars in the mixed stands, the facilitation index (FI), the competition index (CI) and the net interaction index (NI) were calculated as follows: FI =

wf − wn , wn

CI =

wm − wf , wn

NI = FI + CI =

wm − wn , wn

where wf is the dry weight of grain produced per pea plant supported with a frame until full pea maturity, wn is the dry weight of grain produced per pea plant supported with a frame until pea flowering, and wm is the dry weight of grain produced per pea plant grown in mixture with barley. In the same way, the indices were also calculated for the aboveground dry-matter yield per pea plant. The FI measures the aboveground facilitation, which is meant to measure the relative pea response to the support received from barley. The CI measures the pea response to the competition from barley. It was expected that wm would be
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Table 1 Lodging scores according to the Stapper and Fischer (1990) scale for pea cultivars grown in pure stands and in intercrops at full maturity in 2005, 2006 and 2007 at different N application rates in Experiment 1. Year

2005

2006

2007

Treatment

Score

N rate (kg ha−1 )

0

30

60

Mean

Pea cv. Wiato Pea cv. Fidelia Barley + Pea cv. Wiato Barley + Pea cv. Fidelia Mean LSD0.05 N rate LSD0.05 cropping method LSD0.05 interaction N × cropping

72(8.49) 59(7.73) 2(1.66) 1(1.28) 34(4.79)

70 (8.37) 78(8.85) 1(1.21) 2(1.49) 38(4.98) (0.27)

86(9.30) 92(9.63) 7(2.73) 6(2.47) 48(6.03)

76(8.72) 76(8.74) 3(1.87) 3(1.75)

Pea cv. Wiato Pea cv. Fidelia Barley + Pea cv. Wiato Barley + Pea cv. Fidelia Mean LSD0.05 N rate LSD0.05 cropping method LSD0.05 interaction N × cropping

70(8.37) 76(8.75) 5(2.37) 3(1.99) 39(5.37)

Pea cv. Wiato Pea cv. Fidelia Barley + Pea cv. Wiato Barley + Pea cv. Fidelia Mean LSD0.05 N rate LSD0.05 cropping method LSD0.05 interaction N × cropping

68(8.29) 81(9.03) 5(2.37) 4(2.07) 40(5.44)

(0.42) NS 79(8.93) 83(9.15) 4(2.06) 5(2.30) 43(5.61) (0.20)

90(9.53) 92(9.64) 6(2.46) 6(2.48) 49(6.03)

80(8.94) 84(9.18) 5(2.30) 5(2.26)

(0.43) NS 89(9.47) 87(9.37) 6(2.59) 2(1.44) 46(5.72) NS

89(9.47) 92(9.62) 7(2.71) 9(3.04) 49(6.21)

82(9.08) 87(9.34) 6(2.56) 5(2.18)

(0.57) NS

Analysis of variance was performed on square root (x + 0.5) transformed data, and the means are presented in parentheses. The values before the parentheses are the back-transformed means rounded to unity. A score of 0(0.71) indicates no plant lodging, and a score of 100(10.02) indicates completely lodged plants. NS, not significant.

opposite was true in 2006 (Table 2). No significant difference in the RYb was found in 2007. The relative grain yields of the pea cultivars (RYp ) exceeded unity in 2005, showing a net facilitative effect of barley on pea (Fig. 3). Wiato was facilitated more than Fidelia at the highest nitrogen fertilizer treatment. In 2006 when nitrogen was applied at a rate of 30 and 60 kg of N ha−1 , the RYp of both pea cultivars was less than 0.7, which indicated a negative response of the legume when intercropped with barley. The same was true for the highest

2005

Grain yield (t ha-1)

6

N rate in 2007 (data not shown). In 2006 at 0 kg of N ha−1 , the relative grain yield of Wiato was significantly higher than that of Fidelia. The relative grain yield of the latter cultivar significantly exceeded that of Wiato in 2007 irrespective of the N supply (Table 2). The LER calculated using the grain yields exceeded unity during the experimental period, which demonstrated the advantage of the mixtures over the sole crops (Fig. 3 and Table 2). The mixture of the barley with the cultivar Wiato better utilized the available resources than that of the barley with Fidelia at the highest N rate

2006

6

5

5

5

4

4

4

3

3

2

2

1

1

Barley Wiato Fidelia Barley + Wiato Barley + Fidelia

3

2

1

0

0 0

30

60

2007

6

0 0

30

60

0

30

60

N application rate (kg ha-1) Fig. 2. Grain yield of barley, pea cultivars and barley–pea intercrops in 2005, 2006 and 2007 at different N application rates in Experiment 1. Vertical bar represents LSD0.05 values for the comparison of crop yields within a given N application rate.

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2006 2.0

1.5

1.5

RYp

RYp

2005 2.0

1.0

0.5

0.0

1.0

0.5

0.0

0.5

1.0

1.5

2.0

0.0

0.0

0.5

RYb

1.0

1.5

2.0

RYb

Fig. 3. Relative yield of barley (RYb ) and pea (RYp ) and the land equivalent ratio (LER) calculated on the basis of grain yields in 2005 and 2006 in Experiment 1 at different N application rates (circles, triangles and squares are 0, 30 and 60 kg of N ha−1 , respectively). Open and closed symbols represent the barley–Wiato and barley–Fidelia intercrop, respectively. Bars represent the LSD0.05 for the RY and LER comparisons within a given N application rate, with the horizontal, vertical and diagonal bars representing the RYb , RYp and LER comparisons, respectively. No significant difference was detected for RYb in 2006 or for any index in 2007.

Table 2 Relative yield of barley (RYb ) and pea (RYp ), and the land equivalent ratio (LER) calculated on the basis of grain yields in 2005, 2006 and 2007 in Experiment 1. Year

Treatment

RYb

RYp

LER

shown). The nitrogen fertilizer rate did not affect the competitive balance index in 2005 and 2007. In 2006, the competitive dominance of barley in the intercrop was higher at 30 kg of N ha−1 than at the other N fertilization levels (Table 3).

2005

Barley + Pea cv. Wiato Barley + Pea cv. Fidelia LSD0.05

0.43 0.44 NS

1.58 1.41 0.16

2.01 1.86 0.14

3.2. Experiment 2

2006

Barley + Pea cv. Wiato Barley + Pea cv. Fidelia LSD0.05

0.61 0.53 0.07

0.71 0.65 NS

1.32 1.18 0.09

2007

Barley + Pea cv. Wiato Barley + Pea cv. Fidelia LSD0.05

0.51 0.54 NS

0.70 0.83 0.12

1.22 1.37 0.12

Means are averaged over N application rates. NS, not significant.

in 2005 and at 0 kg of N ha−1 in 2006. The barley–Fidelia mixture was more effective than the barley–Wiato mixture in 2007 when averaged over the N rates (Table 2). 3.1.4. Competitive balance index Pea outcompeted barley in 2005 (Cb < 0), but in 2006 and 2007, the cereal was a better competitor than the legume species (Table 3). The competitive ability of both pea cultivars was similar in all three years, except that the competitive ability of Wiato was higher than that of Fidelia at 0 kg of N ha−1 in 2005 (data not Table 3 Competitive balance index (Cb ) calculated on the basis of grain yields in 2005, 2006 and 2007 in Experiment 1. Treatment Stand Barley + Pea cv. Wiato Barley + Pea cv. Fidelia LSD0.05 N rate (kg ha−1 ) 0 30 60 LSD0.05 NS, not significant.

2005

2006

2007

−0.48 −0.30 NS

0.71 0.63 NS

0.53 0.42 NS

−0.36 −0.55 −0.27 NS

0.43 0.90 0.69 0.15

0.31 0.48 0.63 NS

3.2.1. Interaction indices for grain dry-matter yield per pea plant In 2005, the facilitation index (FI) for grain dry-matter yield per pea plant had unexpectedly negative values for certain treatments (Table 4). The FI did not differ between the pea cultivars in 2005, and when averaged over the cultivars, it was highest at 30 kg of N ha−1 . The competition index (CI) was lower for the cultivar Fidelia than for Wiato at 30 kg of N ha−1 but not at the other N fertilizer rates in 2005 (data not shown). For the net interaction index (NI) in 2005, the absence of a significant difference between the pea cultivars shows that the cultivars responded similarly to the barley in the intercrop mixture. In 2006, the FI for the grain dry-matter yield per Fidelia plant was higher than that for Wiato (Table 4). Irrespective of the pea cultivar, the index was the highest at the highest fertilizer rate. Compared to 0 kg of N ha−1 , the CI for both N fertilizer rates decreased significantly in 2006, but the response of the pea cultivars to the competition from barley was similar. An above-zero CI when no N fertilizer was applied suggests that there were other facilitative effects of the barley on pea than those resulting from plant support. The NI shows that the barley intercropped with pea facilitated the grain production of Fidelia but not Wiato, which showed a net negative response. Averaged over the cultivars, a net facilitation in per plant grain production occurred in 2006 with no N fertilization, whereas net competition was observed at 30 and 60 kg of N ha−1 . The Fidelia pea cultivar responded better than the Wiato cultivar to plant support at 0 and 60 kg of N ha−1 in 2007 as far as the grain production per plant is concerned, but no significant difference in the FI was found at 30 kg of N ha−1 (Fig. 4). The CI was lower for Fidelia than for Wiato at 0 and 60 kg of N ha−1 , but the index did not differ between the pea cultivars at 30 kg of N ha−1 . In 2007, the CI for the grain production per Wiato pea plant was above zero without N fertilization. When averaged over the N rates in 2007, the NI was higher for the Fidelia than for the Wiato cultivar (Table 4).

M. Podgórska-Lesiak, P. Sobkowicz / Field Crops Research 149 (2013) 95–104

101

Table 4 Facilitation index (FI), competition index (CI) and net interaction index (NI) calculated on the basis of dry-matter grain yield per pea plant in 2005, 2006 and 2007 in Experiment 2. Treatment

2005

Pea cultivar Wiato Fidelia LSD0.05 N rate (kg ha−1 ) 0 30 60 LSD0.05

2006

2007

FI

CI

NI

FI

CI

NI

FI

CI

NI

−0.12 −0.05 NS

−0.18 −0.28 NS

−0.30 −0.33 NS

0.11 0.44 0.22

−0.31 −0.21 NS

−0.20 0.23 0.37

0.25 1.18 0.28

−0.10 −0.62 0.36

0.15 0.56 0.36

−0.25 0.05 −0.04 0.17

−0.14 −0.43 −0.13 NS

−0.39 −0.38 −0.17 NS

0.28 0.10 0.46 0.14

0.30 −0.30 −0.79 0.66

0.58 −0.20 −0.33 0.66

1.22 0.27 0.66 0.24

0.43 −0.62 −0.88 0.70

1.65 −0.35 −0.22 0.70

NS, not significant.

2007

2007 N application rate (kg ha-1) 0

30

2.0

N application rate (kg ha-1) 60

FI

1.5

30

0.6

1.5

60 NI

0.6

0.4

0.4

0.2

0.2

0.0

0

1.0

0.0

0.0

-0.5

-0.5

-1.0

-1.0

-1.5

FI Wiato FI Fidelia CI Wiato CI Fidelia

-2.0

-0.2

-0.2

-0.4

-1.5

CI

CI

0.5 CI

0.5

-2.0

The CI and the NI decreased with an increase in the N fertilizer rate in 2007. The NI exceeded zero at 0 kg of N ha−1 , which showed net facilitation, and the index was below zero for the other N fertilizer rates, which demonstrated net competition. 3.2.2. Interaction indices for aboveground dry-matter yield per pea plant The facilitation index calculated for the aboveground dry-matter yield per pea plant indicated a better response of the Fidelia than the Wiato cultivar to the plant support from barley in all the experimental years (Table 5). By contrast, Fidelia showed a stronger negative response than Wiato to the competition from barley in 2005 and 2007 irrespective of the N fertilizer application. The

-0.4

CI Wiato CI Fidelia NI Wiato NI Fidelia

-0.6

Fig. 4. Facilitation index (FI) and competition index (CI) calculated on the basis of dry-matter grain yield per pea plant in 2007 at different N application rates in Experiment 2. Vertical bars represent the LSD0.05 for FI or CI comparisons within a given N application rate.

NI

1.0 FI

0 2.0

-0.6 CI

Fig. 5. Competition index (CI) and net interaction index (NI) calculated on the basis of aboveground dry-matter yield per pea plant in 2007 at different N application rates in Experiment 2. Vertical bars represent the LSD0.05 for CI or NI comparisons within a given N application rate.

index did not differ between Wiato and Fidelia in 2007 for just the medium N application rate (Fig. 5) or in 2006 when averaged over the N application rates (Table 5). The different response of both cultivars to the facilitation and competition from barley in 2005 and 2007 resulted in similar values of the net interaction index for the cultivars in those years irrespective of the N input. The statistical interactions between the experimental factors show that in 2007, the net interaction index was higher for Wiato than for Fidelia at 0 kg of N ha−1 , whereas the opposite was true at the medium N application rate (Fig. 5). Irrespective of the N input, the NI was higher for Fidelia than for Wiato in 2006 (Table 5).

Table 5 Facilitation index (FI), competition index (CI) and net interaction index (NI) calculated on the basis of aboveground dry-matter yield per pea plant in 2005, 2006 and 2007 in Experiment 2. Treatment

Pea cultivar Wiato Fidelia LSD0.05 N rate (kg ha−1 ) 0 30 60 LSD0.05 NS, not significant.

2005

2006

2007

FI

CI

NI

FI

CI

NI

FI

CI

NI

−0.08 0.06 0.08

−0.09 −0.21 0.08

−0.17 −0.15 NS

0.13 0.25 0.09

−0.18 −0.16 NS

−0.05 0.09 0.11

0.15 0.37 0.06

−0.17 −0.34 0.07

−0.02 0.03 NS

−0.13 0.06 0.03 NS

−0.07 −0.30 −0.09 NS

−0.20 −0.24 −0.06 NS

0.24 0.09 0.23 0.09

0.12 −0.20 −0.44 0.25

0.36 −0.11 −0.21 0.25

0.38 0.14 0.27 0.07

0.06 −0.39 −0.44 0.20

0.44 −0.25 −0.17 0.20

102

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When averaged over the pea cultivars, the FI calculated for the aboveground dry-matter yield per pea plant was lower at the 30 kg of N ha−1 rate than at the other fertilizer rates in 2006 and 2007 (Table 5). The CI and NI decreased with increasing N fertilizer rates in 2006 and 2007. None of the three indices was affected by the N application rate in 2005. 4. Discussion 4.1. Yield advantage of intercrops Experiment 1 showed a yield advantage for both of the barley–pea intercrops over the pure stands in all three years (LER > 1). In 2006, significantly higher grain yields were observed for the mixtures than for the sole crops. This result is usually considered unambiguous evidence for the superiority of intercropping over sole cropping and has been termed “transgressive overyielding” (Fridley, 2001). It was relatively dry in 2006, with total rainfall from May until July of only 85 mm, compared with the long-term average of 209 mm. This resulted in quite low yields of the sole-cropped barley at 0 and 30 kg of N ha−1 , which allowed the overyielding phenomenon to occur. Our data agree with those reported by Hauggaard-Nielsen et al. (2001a), who found higher yields from barley–pea intercrops than from sole crops in an experiment with a low input of mineral N fertilizer. The mixture of barley with the medium-tall Wiato cultivar was more beneficial in terms of grain yield than that with the tall Fidelia cultivar in two out of the three years of Experiment 1. This result suggests that the dry seed type of cultivar Wiato is better adapted to the mixture with barley than the green fodder/dry seed cultivar Fidelia. There are no data in the literature that compare mixtures of barley with pea cultivars similar to those used in our research. In the experiment of Hauggaard-Nielsen and Jensen (2001), the best performing intercrops were those that included leafy, determinategrowth cultivars of pea. Rauber et al. (2001) found the greatest yield advantage using a tall, leafy pea cultivar grown with oats, whereas Semere and Froud-Williams (2001) and Tofinga et al. (1993) did not find mixtures that included leafy pea cultivars to be superior to those containing semileafless ones. 4.2. Aboveground facilitation The mechanical support provided by barley to pea (visible facilitation) prevented the legume from suffering almost complete lodging in all three years of Experiment 1, but the net facilitation of pea by barley in agronomic terms was demonstrated only in 2005. The low yields of the sole-cropped pea contributed to the high RYb values in that year. It is not clear, however, to what extent the weather contributed to this result because variation in the weather conditions had no influence on the lodging pattern of the sole-cropped pea, which remained similar during the experimental years. Most likely, the 109 mm of rainfall that was received in July detrimentally affected the peas. Substitutive designs like the one used in Experiment 1 are invalid to show facilitation when RY is <1.0; nevertheless, facilitation may have existed in the mixtures (Li and Watkinson, 2000; Vandermeer, 1989). Based on the large differences observed each year between the lodging of peas in the pure stands compared with the mixtures (visible facilitation) and based on the results from Experiment 2, we hypothesize that the support received by the peas from barley had a positive effect on the pea yield in all years of Experiment 1. The facilitating effect of physical support during the full flowering to full maturity stage of pea on the performance of the legume was demonstrated in Experiment 2. The positive response of the tall cultivar Fidelia to physical support was greater than the response

of the medium-tall cultivar Wiato. The negative FI values in 2005 show that the peas yielded less (grain and aboveground plant dry matter) with physical support than without it. This may indicate that there is some assimilate cost of vertical growth of the pea plant that is paid bearing aboveground parts such as pods with grain. The cost may be hidden in sole cropping if there is a detrimental effect of lodging on plant performance. This was the case for the peas in 2006 and 2007 in Experiment 2. This issue highlights the difficulty in measuring the yield advantage of any intercrop. Success may result not only from a particular combination of components that permits some emergent property to occur (resource complementarity or facilitation) but also from the degree of failure when the components are grown alone (Mead and Willey, 1980). 4.3. Competition In Experiment 1, high values of the RYp produced negative values of the Cb in 2005, indicating that the pea cultivars outcompeted the barley in the mixtures, whereas in 2006 and 2007, barley was the better competitor. Though most research suggests a better competitive ability of cereals than pea, the opposite results have also been observed. Bedoussac and Justes (2011) demonstrated a greater competitive ability of pea than wheat in a mixture of both species with a fertilizer treatment of 0 kg of N ha−1 . In research of Corre-Hellou et al. (2006) with several barley–pea mixtures, the relative grain yield of pea was higher than unity in one intercrop. Neither Experiment 1 nor 2 demonstrated explicitly which cultivar of pea was the better competitor with barley. The competition index calculated in Experiment 2 showed that when facilitation was excluded, Fidelia was less tolerant than Wiato to competition from barley. The relative grain yields of the pea cultivars in Experiment 1 varied during the experimental years and did not definitively indicate which cultivar was more affected by the competition from barley. Note, however, that the RYp accumulated positive and negative interactions of pea with barley, and thus, it corresponds to the NI in Experiment 2. The latter index shows that a stronger positive response of Fidelia than Wiato to facilitation was counterbalanced by a stronger negative response of Fidelia to competition from barley. Previous research found that pea plant height is the main determinant of the competitive ability of the legume (HauggaardNielsen and Jensen, 2001; Rauber et al., 2001; Spies et al., 2011). We hypothesize that this advantageous trait of the tall cultivar Fidelia compensated for its lower than Wiato grain yield potential observed in the pure stands in Experiment 1. This compensation resulted in similar performance of the cultivars in Experiments 1 and 2 and the inconsistent results during the experimental period. 4.4. Effect of applied N fertilizer Neither experiment produced results that clearly show whether the importance of the supporting role of barley changes with increasing N fertilizer rate. In Experiment 1, the effect of the N fertilizer rate on lodging was relatively weak, and even when no N fertilizer was applied, both pea cultivars lodged severely in the pure stands. This result may suggest that the role of barley as a mechanical support for pea is independent of the N input. Only the results from 2005 with the Wiato cultivar suggest that the importance of the support provided to pea increased with increasing N fertilizer rate, as was shown by the RYp increase. This cultivar was most likely unable to yield more grain in the pure stand with increasing N application due to lodging. The results from Experiment 2 are inconclusive in this respect because the FI calculated based on grain yield was the highest for the different N fertilizer rates each year.

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The grain yield of the barley grown in the pure stand increased strongly in response to the applied N in Experiment 1. Nevertheless, the Cb values provided little evidence that the increased N fertilizer input changed the competitive balance between barley and pea in the two mixtures. This weak effect of the applied N on the competitive ability of the cereal may be explained by the species proportions in the seeded mixture used in this study, in that relatively few barley plants had to withstand physical interference from the pea plants. In addition, the peas were both leafy-type cultivars that most likely worsened light conditions for the cereal. Berntsen et al. (2004) emphasized the importance of the vertical leaf distribution of the components in the barley–pea mixture for determining the outcome of the interspecific competition. Although most research has demonstrated an increased competitive ability with increased N fertilizer for the cereal component intercropped with pea, Chen et al. (2004) observed a decrease in the partial LER for barley biomass with increasing N rate. In their experiment, the number of seeds of each species that was sown in the mixture per unit area was similar to the proportion used in our study. The growth of barley more than that of pea depends on the soil N, and the lack of N fertilizer input severely reduced the negative effect of barley on the legume in Experiment 2. This reduction allowed for the occurrence of additional facilitative effects of the cereal on peas other than physical support. Hauggaard-Nielsen and Jensen (2005) in their review article showed that belowground facilitation in intercrops frequently appears in nutrient-poor soils. The concept that facilitation prevails in infertile environments is also supported by research in plant ecology. Peltzer et al. (1998) observed aboveground facilitation of Agropyron cristatum by shoots of neighboring plant species in the treatment with the lowest soil N level. Belcher et al. (1995) presented a model indicating that facilitation is detected in “high stress/low biomass” sites because the interplant competition is not intense at these sites but increases in sites with “low stress/high biomass” environments. Both experiments demonstrated that the result of the barley–pea interaction in the mixture, when expressed by indices calculated on the basis of grain yield, depends to a large extent upon the behavior of the entangled and fragile canopy of solecropped pea. If lodging occurs, the outcome of the interaction is then dependent on the degree to which the lodging influences grain yield. In 2005, the negative values of the Cb resulted mainly from the low yields of the pure-stand pea. Thus, if facilitation occurs in the intercrop, the Cb does not show only the result of the competition for resources because under these conditions, the Cb overestimates the interspecies competitive interaction and favors the beneficiary component. If there is no negative effect of plant lodging on the pea grain yield in the pure stand, as in Experiment 2 in 2005, then the support provided by barley to pea may become a form of competitive interaction. This situation suggests that pea supported by intercropped barley grows upright at some assimilate cost, as shown by the negative FI values for the pea grain yields. We realize that four pea plants do not form a canopy similar to that occurring under field conditions in which a dense plant stand results in low light conditions for some plants and increases the susceptibility to fungal diseases. Further research is required to study the lodging process and its consequences for the grain yield potential of dense pea stands. Most studies to date have attributed the yield advantage of the barley–pea intercrop to underground phenomena that influence the mechanisms and efficiency of nitrogen capture by the intercrop components. To better examine the role of the mechanical support provided by barley to pea in the intercrop, further research should include treatments that separate the root systems of the cereal and the legume species. This design will exclude belowground facilitation and complementarity in N use in the intercrop.

103

5. Conclusions Our research showed that the mechanical support of pea by barley is an important interaction to consider when analyzing the relationships between these intercropped species. In Experiment 1, barley performed well in the role of benefactor species by effectively preventing the pea cultivars from lodging. Experiment 2 showed that the mechanical support received by pea during the full flowering to full maturity growth stages increased the grain and dry-matter yields per pea plant. The results thus demonstrate that the interaction between barley and pea in the intercrop is complex, in that the response of the legume is the collective result of positive and negative influences received from the cereal. The importance of this type of facilitation is strongly affected by weather conditions, such as the intensity and amount of rainfall during the reproductive growth stages of pea. The weather may strongly affect the fragile canopy of the pure-stand legume, causing severe lodging and reduced grain yield. The research also shows that without N fertilizer input, barley functions more as a benefactor to pea than a competitor. Acknowledgements Certain results in this article were presented in a thesis submitted by Magdalena Podgórska-Lesiak as partial fulfillment of the requirements for a PhD degree. The research was supported by grant no. N310 070 32/2817 from the Ministry of Science and Higher Education, Republic of Poland. We thank Kazimierz Tarkowski and Adam Machocki for field assistance. References Altieri, M.A., 1999. The ecological role of biodiversity in agroecosystems. Agric. Ecosys. Environ. 74, 19–31. Andersen, M.K., Hauggaard-Nielsen, H., Ambus, P., Jensen, E.S., 2004. Biomass production, symbiotic nitrogen fixation and inorganic N use in dual and tricomponent annual intercrops. Plant Soil 266, 273–287. Annicchiarico, P., Iannucci, A., 2008. Adaptation strategy, germplasm type and adaptive traits for field pea improvement in Italy based on variety responses across climatically contrasting environments. Field Crops Res. 108, 133–142. Bedoussac, L., Justes, E., 2011. A comparison of commonly used indices for evaluating species interactions and intercrop efficiency: application to durum wheatwinter pea intercrops. Field Crops Res. 124, 25–36. Belcher, J.W., Keddy, P.A., Twolan-Strut, L., 1995. Root and shoot competition intensity along a soil depth gradient. J. Ecol. 83, 673–682. Berntsen, J., Hauggaard-Nielsen, H., Olsen, J.E., Petersen, B.M., Jensen, E.S., Thomsen, A., 2004. Modelling dry matter production and resource use in intercrops of pea and barley. Field Crops Res. 88, 69–83. Brooker, R.W., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A., Kunstler, G., Liancourt, P., Tielbörger, K., Travis, J.M.J., Anthelme, F., Armas, C., Coll, L., Corcet, E., Delzon, S., Forey, E., Kikvidze, Z., Olofsson, J., Pugnaire, F., Quiroz, C.L., Saccone, P., Schiffers, K., Seifan, M., Touzard, B., Michalet, R., 2008. Facilitation in plant communities: the past, the present, and the future. J. Ecol. 96, 18–34. Bruno, J.F., Stachowicz, J.J., Bertness, M.D., 2003. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119–125. Bulson, H.A.J., Snaydon, R.W., Stopes, C.E., 1997. Effects of plant density on intercropped wheat and field beans in an organic farming system. J. Agric. Sci. Camb. 128, 59–71. Callaway, R.M., 1995. Positive interactions among plants. Botanical Rev. 61, 306–349. Callaway, R.M., Walker, L.R., 1997. Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78, 1958–1965. Chen, C., Westcott, M., Neill, K., Wichman, D., Knox, M., 2004. Row configuration and nitrogen application for barley–pea intercropping in Montana. Agron. J. 96, 1730–1738. Cochran, V.L., Schlentner, S.F., 1995. Intercropped oat and fababean in Alaska: dry matter production, dinitrogen fixation, nitrogen transfer, and nitrogen fertilizer response. Agron. J. 87, 420–424. Corre-Hellou, G., Brisson, N., Launay, M., Fustec, J., Crozat, Y., 2007. Effect of root depth penetration on soil nitrogen competitive interactions and dry matter production in pea–barley intercrops given different soil nitrogen supplies. Field Crops Res. 103, 76–85. Corre-Hellou, G., Dibet, A., Hauggaard-Nielsen, H., Crozat, Y., Gooding, M., Ambus, P., Dahlmann, C., von Fragstein, P., Pristeri, A., Monti, M., Jensen, E.S., 2011.

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