Intercropping soybean and palisade grass for enhanced land use efficiency and revenue in a no till system

Europ. J. Agronomy 58 (2014) 53–62

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Intercropping soybean and palisade grass for enhanced land use efficiency and revenue in a no till system C.A.C. Crusciol a,∗ , A.S. Nascente b , G.P. Mateus c , C.M. Pariz d , P.O. Martins a , E. Borghi e a

São Paulo State University (UNESP), College of Agricultural Science, Department of Crop Science, P.O. Box 237, 18.610-307 Botucatu, São Paulo, Brazil Brazilian Agricultural Research Corporation (EMBRAPA), Rice and Beans Research Center, P.O. Box 179, 75.375-000 Santo Antônio de Goiás, Goiás, Brazil São Paulo Agency of Agribusiness Technology (APTA), P.O. Box 67, 16.900-000 Andradina, São Paulo, Brazil d College of Veterinary Medicine and Animal Science, Department of Animal Nutrition and Breeding, 18.618-970 Botucatu, São Paulo, Brazil e EMBRAPA Fisheries, Aquaculture and Agricultural Systems, Block 103 South, JK Avenue, Acess 01, Lot 17, Ground Floor, Southern Master, 77.015-012 Palmas, Tocantins, Brazil b c

a r t i c l e

i n f o

Article history: Received 23 October 2013 Received in revised form 14 April 2014 Accepted 2 May 2014 Available online 21 May 2014 Keywords: Crop–livestock integration Intercrop Tropical forage Diversification Cerrado

a b s t r a c t Integrated no-till crop and livestock production systems may help rejuvenate degraded pastures, increase land use efficiency (LUE), and increase enterprise revenue. Our objectives were to evaluate: (1) planting date effects on seed yield and nutrient concentration of an early-maturing, no-till system (NTS) soybean (Glycine max) when intercropped with palisade grass (Brachiaria brizantha); (2) dry matter production and protein concentration of the grass pasture after soybean harvest; and (3) overall revenue and LUE for the intercrop system. Experiments were performed during two growing seasons in Botucatu, Brazil using a randomized complete block experimental design. When palisade grass and soybean were sown simultaneously, soybean yield averaged 3.28 Mg ha−1 . Similar seed yields were observed when palisade grass was planted either 30 d after soybean emergence (DAE) (3.29 Mg ha−1 ) or at the soybean reproductive stage R6 (full seed) (3.50 Mg ha−1 ). Monocrop soybean yield averaged 3.50 Mg ha−1 . First cut dry matter forage production was greater when palisade grass was sown at the same time as soybean or 30 DAE of soybean. This indicates that interseeding palisade grass with soybean does not significantly affect soybean nutrition or yield. Intercropping did increase LUE and resulted in 1.6 times more revenue than soybean alone. However, sowing palisade grass at the soybean reproductive stage R6 (full seed) significantly reduced the forage yield compared to early planting. © 2014 Elsevier B.V. All rights reserved.

1. Introduction While global demand for food increases, agricultural expansion faces more stringent environmental preservation demands and sustainability laws aimed to prevent deforestation (Rufino et al., 2006; Satheeshkumar et al., 2011; Nascente and Crusciol, 2012). The Cerrado Region of Brazil encompasses an area of approximately 80 million hectares of cultivated pasture, of which 62.5% exhibits some degree of degradation (Borghi et al., 2013). Integrated crop–livestock systems are characterized by diversification, rotation, and cropping related to grain and animal production within

Abbreviations: NTS, no-tillage system; DAE, days after emergence; NPP, number of pods per plant; NSP, number of seeds per pod; W100, weight of 100 seeds; SY, seed yield; PDMF, palisade grass dry matter. ∗ Corresponding author. Tel.: +55 14 3880 7564; fax: +55 14 3880 7000. E-mail addresses: [email protected] (C.A.C. Crusciol), [email protected] (A.S. Nascente). http://dx.doi.org/10.1016/j.eja.2014.05.001 1161-0301/© 2014 Elsevier B.V. All rights reserved.

the same land area (Tedla et al., 1999; Reda et al., 2005; Sulc and Tracy, 2007; Ryan et al., 2012). Crop–livestock integration can be utilized to simultaneously increase soybean (i.e., food) production and recover degraded pastures without expansion into new agricultural areas (Garcia et al., 2008; Tracy and Zhang, 2008; Maughan et al., 2009; Takin, 2012). Therefore, integrated crop–livestock systems could be a key form of ecological intensification needed for achieving future food security and environmental sustainability. The “Santa Fe System” (Kluthcouski et al., 2003) encourages seed crop production, especially corn (Zea mays L.), sorghum [Sorghum bicolor (L.) Moench], pearl millet [Pennisetum glaucum (L.) R. Br.] and soybean, and interseeding with tropical forages from the Brachiaria and Panicum genera. Those annual grain crops exhibit robust initial growth and development, thereby exerting a high level of competition on the forage and avoiding a significant decrease in crop yield (Kluthcouski et al., 2003). After harvesting the cash crops, forages, if developed properly, can grow quickly and be used to recover degraded pastures using residual fertilizer from the grain crops. Portes et al. (2000) evaluated palisade grass interseeded

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simultaneously with maize, sorghum, pearl millet and rice (Oryza sativa L.) by measuring its regrowth after the cereals were harvested. They observed that the presence of the cereals reduced tiller number, leaf area index, total leaf matter, dry matter of green leaves and stems, and palisade grass growth rate prior to the cereal harvest. Additionally, they noted that the leaf areas of intercropped palisade grass were lower than that of the cereals and that low competition for light from palisade grass favored a good seed yield. Approximately 60–70 d after the cereals were harvested, palisade grass regrowth displayed an herbage yield similar to that of a palisade grass monoculture 70 d after emergence. Without competition, palisade grass can grow rapidly because its stems develop roots when they come in contact with soil and therefore the plant can spread quickly with time (Valle and Pagliarini, 2009). This integrated system is advantageous because it does not change the schedule of agricultural activities and does not require special or costly equipment (Kluthcouski et al., 2003; Crusciol et al., 2010). Furthermore, forage has a dual purpose in this system, as food for cattle in times of drought and as straw to protect soil resources within the NTS (Borghi and Crusciol, 2007). Additionally, intercropping soybean with palisade grass does not typically reduce nutrient concentrations in soybean plants (Crusciol et al., 2010). Borghi et al. (2013) observed that leaf nutrient concentrations of soybean cultivars simultaneously sown with palisade grass were within the expected range. Borghi and Crusciol (2007) also did not observe a reduction in nutrient uptake by corn that was intercropped with palisade grass. As an additional information, it is important to study competition effects between the crops and to evaluate intercrop performance, for this, different competition functions such as the relative yield should be calculated (Agegnehu et al., 2006; Takin, 2012). Simultaneously sowing soybean with palisade grass promotes legume growth by reducing weed incidence. The grass forage also disrupts soybean pest and diseases cycles (Silva et al., 2009). Forages grow quickly and display an aggressive root system that favors nutrient cycling, which improves soil physical properties, increases biological activity and organic matter, and provides a persistent surface residue cover. This residue is important because it can reduce soil erosion, weed growth and, consequently, herbicide application (Rosolem et al., 2004; Crusciol and Soratto, 2007, 2009; Nascente and Crusciol, 2012). Additionally, grass forages benefit from residual fertilizer, biological nitrogen fixation by legumes, soil liming and from the disruption of pest and disease cycles (Kluthcouski et al., 2003). Although sowing corn or sorghum with palisade grass has shown promising results in several studies (Portes et al., 2000; Borghi and Crusciol, 2007; Crusciol et al., 2010), more research is required to elucidate effects of interseeding palisade grass with soybean. This combination is challenging to manage, as it requires knowledge of the optimal time to sow the grass, since it can grow rapidly in some situations and can adversely affect soybean development, harvest or yield (Silva et al., 2009). These authors suggest that adequate forage management is essential for successful intercropping to prevent any interference with the crop. After evaluating the effects of six rates of the herbicide fluazifop-p-butyl in establishing soybean and palisade grass intercropping, they concluded that low doses of herbicide could be used to intercrop soybean and palisade grass. However, the presence of other grass species may invalidate these findings because species such as Brachiaria plantaginea have fast initial growth and can quickly overcome palisade grass. In other cases, a soybean crop may have a quick-closing canopy that shades the grass, causing it to die and hindering recovery of the pasture after grain harvest (Crusciol et al., 2010). According to Silva et al. (2009), precise timing of the herbicide application is essential for managing palisade grass intercropped with soybean. Extremely

late applications, near the soybean flowering stage, may not allow the grass to recover due to shading, whereas with early applications, weeds may emerge and decrease soybean yield. Therefore, studies designed to optimize sowing palisade grass with soybean need to be performed. Specifically, soybean losses must be avoided while promoting high forage biomass production by the forage for use in animal grazing and/or straw residues for NTS. Our objectives were to evaluate: (1) nutrient concentration and seed yield of an early-maturing NTS soybean cultivar ‘Embrapa 48’, intercropped with palisade grass cv. ‘Marandu’ sown into the intercrop at different stages of soybean growth; (2) dry matter production and protein concentration of the palisade grass pasture after soybean harvest; and (3) land use efficiency (LUE) and revenue generated by intercropping. 2. Material and methods 2.1. Site description The experiment was performed in Botucatu, State of São Paulo, in southeastern Brazil (48◦ 23 W; 22◦ 51 S; 765 m above sea level) during the 2005–2006 and 2006–2007 growing seasons. The soil (a clay loam, kaolinitic, thermic Typic Haplorthox) (FAO, 2006) contained 630, 90 and 280 g kg−1 of clay, silt and sand, respectively, had been managed for 5 years in a NTS consisting of 1st year – corn in the summer and oat (Avena sativa L.) in the fall; 2nd year – soybean in the summer and corn in the fall; 3rd year – corn in the summer and oat in the fall; 4th year – soybean in the summer and oats in the fall; and 5th year – corn in the summer, oat in the fall, and pearl millet in the spring. The climate, according to the Koppen classification, is CWa that is tropical with a dry winter and a hot, rainy summer. The long-term annual temperatures (1956–2006) includes a maximum, minimum, and average of 26.1 ◦ C, 15.3 ◦ C and 20.7 ◦ C, respectively. Average annual rainfall is 1359 mm. Actual rainfall and temperature measured during the experimental period are presented in Fig. 1. In the 2005–2006 growing season, the amount of rainfall (1212 mm, Fig. 1) was ∼10% less than the long-term (1956–2006) average (1359 mm). The temperature (20.3 ◦ C) was also cooler than the long-term average (20.7 ◦ C), with the lowest temperatures in June (16.0 ◦ C) and July (15.0 ◦ C). During the second growing season (2006–2007), the annual precipitation (1720 mm) was ∼27% higher than the long-term average. The annual average temperature of 20.8 ◦ C was also similar to the long-term average, with the lowest temperatures occurring in May (17.0 ◦ C) and June (18.0 ◦ C). Before initiating the experiment, soil chemical characteristics were determined (0–20 cm) according to van Raij et al. (2001).

Fig. 1. Temperature and rainfall during the study period, which includes the first year, from October 2005 to September 2006, and the second year, from October 2006 to September 2007.

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Results for 2005–2006 and 2006–2007 showed pH values of 5.0 and 5.2; total soil organic matter of 25 and 26 g kg−1 ; P (resin) of 19 and 19 mg kg−1 ; exchangeable K, Ca, Mg, and total acidity at pH 7.0 (H+Al) of 2.6 and 3.1, 34 and 34, 16 and 18, and 46 and 47 mmolc kg−1 , respectively; and base saturations of 530 and 586 g kg−1 , respectively. Soil pH was determined using a 0.01 mol L−1 CaCl2 suspension (1:2.5 soil/solution). Exchangeable Al was extracted with neutral 1 mol L−1 KCl in a 1:10 soil/solution ratio and determined by titration with a 0.025 mol L−1 NaOH solution. P and exchangeable Ca, Mg, and K were extracted with an ion exchange resin and determined by atomic absorption spectrophotometry. Base saturation values were calculated using the results obtained using exchangeable bases and a total acidity at pH 7.0 (H+Al) (van Raij et al., 2001). 2.2. Experimental design and treatments The experimental design was a randomized block with four treatments and six replications. Treatments consisted of four cropping systems, one monocrop and three intercrops: 1 – soybean as control, 2 – sowing ‘Marandu’ palisade grass intercropped simultaneously with soybean, 3 – oversowing palisade grass 30 DAE of soybean, and 4 – oversowing palisade grass at the soybean reproductive stage R6, full seed (Fehr and Caviness, 1977). In addition, to evaluate the effect of the soybean on the forage production, at the time intercrop forages were sown, monoculture forage plots were sown in each replication using the same practices. Each plot consisted of 10, 20-m-long rows of soybean, spaced at 0.45 m, thus providing a total area of 90 m2 . The monoculture forage plots had the same size and same number of replications of the others treatments. However, the forage monoculture plots were used only for the intercropping competition factors calculation. 2.3. Crop management The soybean cultivar ‘Embrapa 48’ (early cycle, maturity group 6.8) was sown into approximately 10 Mg ha−1 of millet straw on November, 25th 2005 and October, 28th 2006, at a 3-cm depth and density of 350,000 seeds ha−1 using no-till seeding (Semeato, model Personale Drill 13, Passo Fundo, RS, Brazil). All treatments in both years were fertilized in the furrows with 24 kg ha−1 of N as urea, 37 kg ha−1 of P as triple superphosphate and 33 kg ha−1 of K as potassium chloride. The soybean was cultivated according to crop needs (Embrapa Soja, 2006). Weeds were desiccated twice, 10 d before and immediately before soybean sowing by applying glyphosate [Isopropylamine salt of N-(phosphonomethyl)glycine] at a rate of 1.92 kg ha−1 acid. This was equivalent to using a boom sprayer with a spray volume of 250 l ha−1 . During herbicide application, we experienced weak winds, a temperature of approximately 25 ◦ C and a relative humidity of approximately 80%. Herbicide was applied only after the dew on the cover crop leaves dried and at no other point during the soybean lifecycle. The fungicide carboxin (5,6-dihydro-2-methyl-1,4-oxathiin3-carboxamide) + thiram (tetramethylthiuram disulfide) was applied to the soybean seeds at a dose of 60 g of active ingredient (a.i.) to 100 kg of seeds. Soybean seeds were then inoculated with Bradyrhizobium japonicum (SEMIA 5079 – CPAC 15 and SEMIA 5080 – CPAC 7) at a dose of 250 g of the inoculant per 50 kg of soybean seeds. The insecticide Lambda-cyhalothrin [␣cyano-3-phenoxybenzyl3-(2-chloro-3,3,3-trifluoroprop-1-enyl)2,2-dimethylcyclopropanecarboxylate, a 1:1 mixture of the (Z)(1 R, 3 R), S-ester and (Z)-(1S, 3S), R-ester] was applied at 7.5 g a.i. ha−1 at 32 and 64 DAE in both years. In the final application, the insecticide was mixed with the fungicide tebuconazole (␣-[2-(4-chlorophenyl)ethyl]-␣-(1,1-dimethylethyl)-1H-1,2,4triazole-1-ethanol) at a dose of 200 g a.i. ha−1 .

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When palisade grass and soybean were sown simultaneously in the intercropping, grass seeds were also sown at a density of 3.4 kg ha−1 of seeds. They were mixed with soybean fertilizer and sown at the same time as soybean. Palisade grass was planted at a depth of 8 cm, as described by Borghi et al. (2013). For other intercropping treatments, forage seeds were broadcast on the surface at a density of 6.8 kg ha−1 of seeds. The amount of seeds was increased because they were spread on the soil surface (Kluthcouski et al., 2003) rather than incorporated. Soybean and palisade grass seedlings emerged on average of 2 years 6 and 13 d after sowing, respectively, when the two species were sown simultaneously in the intercrop. When palisade grass was oversown 30 DAE of soybean (December, 31st 2005 and December, 11th 2006 for the 1st and 2nd growing seasons, respectively), the grass emerged in 7 d. Emergence was aided by 22 mm of rainfall on the 1st d after sowing and 16 mm of rainfall on the 3rd d after sowing in the 1st and 2nd growing seasons, respectively. When palisade grass was oversown at the soybean reproductive stage R6 (full seed) (March, 6th 2006 and February, 9th 2007 for the first and second growing season, respectively), seedlings emerged 8 d afterwards having received 12 mm of rain on the 3rd d after sowing and 31 mm on the 2nd d after sowing in the 1st and 2nd growing seasons, respectively. Furthermore, the average growing season (length of time from emergence to harvest) was 114 d in 2005–2006 (March, 24th 2006) and 119 d in 2006–2007 (February, 20th 2007). 2.4. Sampling Soybean leaf samples were collected from the upper third trifoliate at the R2 growth stage, full bloom (Fehr and Caviness, 1977). Petioles from 30 plants per plot were collected as proposed by Ambrosano et al. (1996), washed and then dried under forced air circulation at 65 ◦ C for 72 h before grinding and analyzing the samples for chemical composition. Concentrations of N, P, K, Ca, Mg, and S were determined using methods described by Malavolta et al. (1997). Nitrogen was extracted with H2 SO4 , and the other nutrients were extracted with a nitro-perchloric solution. The N concentration in the digested solution was determined by Kjeldahl analysis. The P, K, Ca, Mg and S concentrations were determined by atomic absorption spectrophotometry. After eliminating 0.50 m on each side of the plots, soybeans were harvested from the four central rows using a mechanical harvester. After collecting plot yields, the remainder soybean of the area was harvested, thereby removing all of the soybean residue. This residue was used to evaluate N content in the aboveground biomass of soybean following the methods proposed by Ambrosano et al. (1996). Soybean residue was washed and then dried under forced air circulation at 65 ◦ C for 72 h before grinding and analyzing the samples for N concentration using methods described by Malavolta et al. (1997). Grass forage within the entire plot was cut at a height of 0.20 m above the soil and, removed from the area. Aboveground biomass and plant density were recorded. Soybean seed was weighed and yields were corrected to a moisture content of 130 g kg−1 . Agronomic characteristics including the final plant population (calculated per ha from the number of plants in the two, 8-m rows within the center of each plot), height of the first pod insertion, plant height, number of pods per plant, number of seeds per pod (evaluated for 10 randomly chosen plants per plot), and the 100 seed weight (calculated from eight random samples per plot). In June 23rd and October 23rd in 2006, and June 1st and October 1st in 2007, palisade grass dry matter production was evaluated. All herbage within a 2 m2 area per plot was cut at a 25-cm stubble height with manual mechanical rotary mowers. The collected material was dried by forced air circulation

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at 65 ◦ C for 72 h. Crude protein was evaluated by extracting N with H2 SO4 , and determining the concentration in the digested solution by Kjeldahl analysis. Crude protein was expressed as N × 6.25 (Malavolta et al., 1997).

2.5. Statistical analyses For all variables, an analysis of variance and F probability test were performed. The cropping system and year were considered fixed effects. A comparison of means was performed with Tukey’s test (p ≤ 0.10), using the statistical program SISVAR (Ferreira, 1999).

2.6. Economic evaluation An economic evaluation of each cropping system was conducted by computing the cost per hectare to produce soybean either alone or intercropped with palisade grass (CONAB, 2010). The only difference between the two systems was forage seed cost and deployment price. For intercropping, we used the same process to sow both soybean and grass seed simultaneously, so seed cost was the only additional cost. Gross returns for soybean were calculated by multiplying the average seed yield (kg ha−1 ) by the price per kg. To compute economic value for the forage, we computed its value for increasing animal weight gain. According to Borghi et al. (2013), using pasture within an integrated crop and livestock system, it is possible to produce up to 5 kg of live cattle weight ha−1 d−1 . Assuming a 50% yield from the carcass weight, that means 2.5 kg of meat d−1 ha−1 could be produced depending upon the amount of palisade grass dry matter and its protein concentration, which should be above 70 g kg−1 (Van Soest, 1994). In this study, producing soybean + palisade grass sown simultaneously resulted in a forage yield of 18.9 Mg ha−1 when summed for the two cuts; overseeding palisade grass oversowing 30 d after soybean emergence produced 18.4 Mg ha−1 of forage biomass; and overseeding at the soybean reproductive stage R6 (full seed) produced 14.2 Mg ha−1 of biomass. Based on these forage yield estimates, meat yield for the three systems was estimated at 2.50, 2.43 and 1.88 kg d−1 ha−1 , respectively. Having established the potential daily meat production for the three systems, the next step was to estimate the length of time suitable for animal grazing. We considered a time frame of 365 d including a 60-d waiting period between soybean harvest and animal grazing of the palisade grass. Coupled with an average soybean life cycle of 114 d, this resulted in an animal grazing period of 191 d (i.e., 365 − 114 − 60) for all of the treatments. Multiplying the animal grazing period (191 d) by potential meat production 1.88–2.50 kg d−1 ha−1 provided a projection for kilos of meat ha−1 d−1 for each cropping system. Gross return per ha for the integrated crop and livestock system was calculated using: [(price per kg × soybean seed yield) + (yield of meat × price per kg)]. Net return per ha was calculated by subtracting costs per ha from the gross returns. Price estimates were obtained using the Brazilian national average beef and soybean prices for June 2013. Values were converted to Euro (Agrolink, 2013).

and total RNY were calculated analogously based on the harvested N yields as proposed by Lüscher and Aeschlimann (2006). 3. Results 3.1. Weather conditions The soybeans crop received 734 mm of rainfall in the first growing season and 741 mm in the second. The palisade grass received different amounts of water from rain depending on the timing of sowing. Palisade grass sown simultaneously with soybean, 30 DAE of soybean, or at the soybean reproductive stage R6 (full seed) received 934, 770, or 280 mm of rainfall, respectively, prior to the first cutting in June of the first growing season. During the second growing season, the palisade grass treatments received 1189, 996, or 539 mm of rainwater, respectively, before the first cutting in June. Between cuttings (from June to October), palisade grass in the first growing season received less rainfall (about 120 mm) than in the second growing season (about 330 mm) (see Fig. 1). 3.2. Leaf nutrient concentration Simultaneous sowing of palisade grass with soybean (62.3 g kg−1 ) and oversowing palisade grass 30 DAE of soybean (60.4 g kg−1 ) increased the soybean leaf N concentration compared with that of the soybean monoculture (52.0 g kg−1 ) (Tables 1 and 2). The results also indicate that the S concentrations in soybean tissue when palisade grass was sown simultaneously in the intercrop (3.5 g kg−1 ) or 30 DAE of soybean (3.5 g kg−1 ) were greater than from monocultured soybeans (2.7 g kg−1 ). The other nutrients (P, K, Ca and Mg) were not affected by the different sowing parameters. 3.3. Agronomic characteristics Treatments did not influence the final plant population at harvest, the height of the first pod, or the plant height (Tables 1 and 3). The palisade grass treatments did not influence the number of pods per plant, the number of seeds per pod, the weight of 100 seeds or the seed yield of the soybean crops (Table 4). Soybean yield averaged 2.94 Mg ha−1 for the 2005–2006 season and 3.84 Mg ha−1 in 2007–2008 (Table 4). 3.4. Forage dry matter production and crude protein As we did not have year effect on the variable palisade grass forage dry matter (PFDM), we showed the average of two growing seasons (Table 5). The only exception was in the second cutting, when in the first growing season (9.6 Mg ha−1 ) differed from the second growing season (10.7 Mg ha−1 ). The average of simultaneous intercropping of palisade grass with soybean (8.4 Mg ha−1 ) and the sowing of palisade grass at 30 DAE of soybean (8.1 Mg ha−1 ) produced the most PFDM in the 1st cut performed in June (approximately 70 d after soybean harvesting) than in the treatment when palisade grass was oversowing at the soybean reproductive stage R6 (full seed). At the 2nd cut in October, there were no differences in the forage dry matter production among all cropping systems. The crude protein concentration in palisade grass leaves did not differ significantly between treatments.

2.7. Intercropping competition factors 3.5. Economic evaluations Relative crop yield (RY) in relation to monoculture yields for each species was calculated by dividing aboveground biomass in the mixture by that in monoculture. Total RY of the mixture was obtained by adding the RY of both species. Relative N yield (RNY)

Soybean sown alone had the lowest net realization in the sum of 2 years, D 1733 (Table 6). Simultaneous intercropping yielded the highest net realization (D 2717) followed by the treatment

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Table 1 ANOVA (F probability) significance for Nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg) and sulfur (S) leaf concentrations, evaluated at the R2 reproductive stage, plant population, height of first pod, plant height, number of pods per plant (NPP), number of seeds per pod (NSP), weight of 100 seeds (W100), seed yield (SY), relative crop yield (RCY) and nitrogen crop yield (NCY) of soybeans plants cultivated at different sowing times with palisade grass and forage dry matter production and crude protein concentration in palisade grass. Factors (freedom degree – FD)

F probability N

P

K

Blocks (FD = 5) Year (FD = 1) Treatment (FD = 3) Year × treatment (FD = 3)

0.9345 0.3211 0.0408 0.5561

0.8823 0.4957 0.2193 0.6719

0.8349 0.5011 0.1602 0.3945

Factors (freedom degree – FD)

F probability Ca

Mg

S

Blocks (FD = 5) Year (FD = 1) Treatment (FD = 3) Year × treatment (FD = 3)

0.7319 0.4781 0.7066 0.8155

0.7886 0.5941 0.6937 0.6584

0.9046 0.5749 0.0907 0.6231

Factors (freedom degree – FD)

F probability

Blocks (FD = 5) Year (FD = 1) Treatment (FD = 3) Year × treatment (FD = 3) Factors (freedom degree – FD)

Population

Height of first pod

Height of plants

0.4470 0.6664 0.7635 0.7187

0.3471 0.7633 0.2670 0.5931

0.6843 0.5854 0.6704 0.6002

F probability NPP

NSP

W100

SY

Blocks (FD = 5) Year (FD = 1) Treatment (FD = 3) Year × treatment (FD = 3)

0.6395 0.0264 0.0642 0.5722

0.9441 0.6277 0.3949 0.7438

0.2190 0.4971 0.4570 0.3846

0.6662 0.0008 0.4194 0.4377

Factors (freedom degree – FD)

F probability Forage dry matter a

Blocks (FD = 5) Year (FD = 1) Treatment (FD = 2) Year × treatment (FD = 2) Factors (freedom degree – FD)

Crude protein

1st

2nd

1st

2nd

0.1330 0.3415 0.0002 0.3561

0.3020 0.0088 0.1627 0.6486

0.5725 0.3865 0.7563 0.6883

0.4382 0.0261 0.5898 0.3714

F probability RCY

Blocks (FD = 5) Year (FD = 1) Treatment (FD = 2) Year × treatment (FD = 2) a

RNY

Soybean

Palisade grass

Total

Soybean

Palisade grass

Total

0.2578 0.3444 0.1328 0.5135

0.2061 0.4185 0.0371 0.4948

0.2111 0.6387 0.0967 0.5555

0.3513 0.4659 0.6819 0.8564

0.1704 0.0415 0.0711 0.1594

0.2569 0.0683 0.0989 0.1852

First and second assessments were performed in June and October, respectively, after the soybean harvest.

oversowing at 30 DAE of soybean (D 2651) and oversowing at the soybean reproductive stage R6 (full seed) (D 2529).

4. Discussion 4.1. Weather conditions

3.6. Relative crop and nitrogen yield Regarding relative crop yield and relative nitrogen yield, in the first growing season soybean provided similar values of seed yield in all treatments (Table 7). On the other hand, in the second growing season the intercrop grown at 30 d after soybean sowing had the lowest seed yield, which was 10.2% less than the soybean monoculture. In both years palisade grass had the lowest relative yield under the intercrop grown simultaneously. Regarding nitrogen yield, soybean plants uptake higher amount of nitrogen than forage plants in all treatments.

The amounts of rainfall received by soybeans were slightly above the range (689–731 mm) considered to be sufficient for the cash crop development without water stress (Embrapa Soja, 2006). On the other hand, grass that was sown later received a smaller amount of water, which may have directly affected the amount of dry matter produced. Pacheco et al. (2008) stated that oversowing palisade grass at the soybean reproductive stages R6–R7 was quite risky, suggesting that success depends on a series of rainfall events until the grass is well rooted. However, we observed that there was sufficient rainfall in both growing seasons

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Table 2 Nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg) and sulfur (S) leaf concentrations, evaluated at the R2 reproductive stage from soybean plants cultivated at different sowing times with palisade grass in two growing seasons. Treatments

N (g kg−1 )

P (g kg−1 )

K (g kg−1 )

Crop systemA Monoculture Simultaneously Oversowing – 30 DAE

52.0 bB 62.3 a 60.4 a

3.0 a 3.4 a 3.3 a

20.9 a 24.4 a 24.5 a

Growing seasons 05–06 06–07

57.5 a 56.8 a

3.1 a 3.2 a

21.8 a 23.4 a

Treatments

Ca (g kg−1 )

Mg (g kg−1 )

S (g kg−1 )

Crop systemA Monoculture Simultaneously Oversowing – 30 DAE

8.5 a 8.2 a 8.4 a

5.1 a 4.8 a 4.9 a

2.7 b 3.5 a 3.5 a

Growing seasons 05–06 06–07

8.9 a 7.8 a

5.2 a 4.7 a

3.2 a 3.1 a

A Monoculture: soybean monoculture; simultaneously: palisade grass was sown simultaneously with soybeans; oversowing: palisade grass was oversown 30 d after the emergence (DAE) of soybeans. B Values followed by the same lowercase letter, presented vertically, are not significantly different at p ≤ 0.10 according to Tukey’s test.

Table 5 Forage dry matter production (FDMP) and crude protein concentration in palisade grass pasture as a function of sowing palisade grass with soybeans in two growing seasons. Treatments

FDMP

Crude protein

First cutB (Mg ha−1 )

Second cut (Mg ha−1 )

First cut (g kg−1 )

Crop systemA Simultaneously Oversowing – 30 DAE Oversowing R6

8.4 aC 8.1 a 4.6 b

10.5 a 10.3 a 9.6 a

109 a 107 a 111 a

Growing seasons 05–06 06–07

7.0 a 7.2 a

9.6 b 10.7 a

111 a 107 a

Second cut (g kg−1 )

139 a 136 a 139 a 13.5 b 14.1 a

A Simultaneously: palisade grass was sown simultaneously with soybeans; oversowing: palisade grass was oversown 30 d after the emergence (DAE) of soybeans; Oversowing R6: palisade grass was oversown at the soybean reproductive stage R6 (full seed). B First and second assessments were performed in June and October, respectively, after the soybean harvest. C Values followed by the same lowercase letter, presented vertically, are not significantly different at p ≤ 0.10 according to Tukey’s test.

to allow the seeds to germinate and the palisade grass to properly develop. 4.2. Leaf nutrient concentration

Table 3 Plant population, height of first pod and plant height of soybeans cultivated at different sowing times with palisade grass in two growing seasons. Plant population (n◦ × 1000 ha−1 )

Height of first pod (cm)

Height of plants (cm)

Crop systemA Monoculture Simultaneously Oversowing – 30 DAE Oversowing R6

316 aB 317 a 317 a 316 a

16.6 a 17.9 a 17.8 a 17.0 a

65.7 a 63.9 a 64.9 a 64.5 a

Growing seasons 05–06 06–07

317 a 317 a

17.3 a 17.3 a

61.8 a 67.8 a

Treatments

A Monoculture: soybean monoculture; simultaneously: palisade grass was sown simultaneously with soybeans; oversowing: palisade grass was oversown 30 d after the emergence (DAE) of soybeans; Oversowing R6: palisade grass was oversown at the soybean reproductive stage R6 (full seed). B Values followed by the same lowercase letter, presented vertically, are not significantly different at p ≤ 0.10 according to Tukey’s test.

Table 4 Number of pods per plant (NPP), number of seeds per pod (NSP), weight of 100 seeds (W100) and seed yield (SY) in soybean plants cultivated at different sowing times with palisade grass in two growing seasons. Treatments

NPP (n◦ )

NSP (n◦ )

W100 (g)

SY (Mg ha−1 )

Crop systemA Monoculture Simultaneously Oversowing – 30 DAE Oversowing R6

33.7 aB 32.4 a 30.1 a 34.1 a

2.1 a 1.9 a 2.1 a 2.1 a

19.3 a 18.6 a 18.9 a 18.7 a

2.97 a 2.91 a 2.96 a 2.93 a

Growing seasons 05–06 06–07

27.4 b 38.0 a

2.0 a 2.1 a

19.5 a 18.3 a

2.94 b 3.84 a

A Monoculture: soybean monoculture; simultaneously: palisade grass was sown simultaneously with soybeans; oversowing: palisade grass was oversown 30 d after the emergence (DAE) of soybeans; Oversowing R6: palisade grass was oversown at the soybean reproductive stage R6 (full seed). B Values followed by the same lowercase letter, presented vertically, are not significantly different at p ≤ 0.10 according to Tukey’s test.

Despite some differences among treatments, foliar levels were all within the range considered appropriate for the soybean crop (Ambrosano et al., 1996; Malavolta et al., 1997; Embrapa Soja, 2006). Palisade grass did not negatively affect soybean nutrient concentrations in any of the treatments. For some cases, such as N and S, intercropping increased their concentrations in soybean leaves. This result is supported by previous reports that demonstrated an increase in cash crop leaf concentrations when intercropped with palisade grass (Borghi and Crusciol, 2007; Crusciol et al., 2010). However, the authors did not explain why concentrations increased and we currently do not have an explanation for this response. 4.3. Agronomic characteristics The observed plant population (317,000 plants ha−1 ) was similar to the population size reported by Kluthcouski et al. (2003) for both soybean monocultures and soybeans sown with palisade grass evaluated in different locations. There was not significant effect of the intercropping in the height of the first pod and plant height. Pereira et al. (2011) also observed that the addition of signal grass 25 DAE of soybean had no effect on the height of the first pod compared with a soybean monoculture under a no-tillage system. The observed plant height was also similar to that reported by Giarola et al. (2009) for the cultivar Embrapa 48 (63 cm) that was grown in a soybean monoculture. They reported that this feature is predominantly affected by the genetic factors of each cultivar. Notably, if competition existed between the soybeans and the grass, such attributes would likely be altered in intercropped soybeans when compared with the soybean monoculture. In addition, according to Embrapa Soja (2006) when the soybean plant height is smaller than 65.0 cm it will need some degree of adaptation in the harvest machinery. In our study this variable ranged from 63.9 to 65.7, which could need some adaptation of the harvest machinery. According to Yokomizo et al. (2000), the first pod must be at least 12 cm tall to enable proper mechanical harvesting of soybean. In this study, the height of the first soybean pod ranged from 16.6 to 17.9 cm, and did not differ among treatments (Table 3) and

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59

Table 6 Economic evaluation of the intercropping systems sole soybean and intercropped with palisade grass in two growing seasons. Crop systemsa

Costb (D ha−1 )

2005/2006 Monoculture Simultaneously Oversowing – 30 DAE Oversowing R6

458 474 495 495

2006/2007 Monoculture Simultaneously Oversowing – 30 DAE Oversowing R6

458 474 495 495

Crop systemsa

GYc (kg ha−1 )

Totald (D)

Meate (kg ha−1 )

Totalf (D)

Grossg (D ha−1 )

Neth (D ha−1 )

2970 2910 2960 2930

1158 1077 1095 1084

– 477.5 464.1 359.1

– 621 603 467

1158 1698 1699 1551

700 1224 1204 1056

4030 3640 3620 4060

1491 1347 1339 1502

– 477.5 464.1 359.1

– 621 603 467

1491 1968 1943 1969

1033 1497 1448 1474

Sum of 2 year

Monoculture Simultaneously Oversowing – 30 DAE Oversowing R6

Gross

Net

2649 3665 3641 3520

1733 2717 2651 2530

a Monoculture: soybean monoculture; simultaneously: palisade grass was sown simultaneously with soybeans; oversowing: palisade grass was oversown 30 d after the emergence (DAE) of soybeans; oversowing R6: palisade grass was oversown at the soybean reproductive stage R6 (full seed). b Cost means the cost to produce sole soybean or soybean intercropped, the only difference was the forage seeds cost. c GY means the soybean grain yield. d Total = kg of soybean × D 0.39. e kg of meat produced = 191 × 2.50 kg d−1 ha−1 for treatment intercropping soybean x palisade grass sown simultaneously, 191 × 2.43 kg d−1 ha−1 for palisade grass oversowing at 30 DAE of soybean, 191 × 1.88 kg d−1 ha−1 for palisade grass oversowing at R6 soybean reproductive stage. f Total kg of meat × D 1.3. g Gross means gross realization per ha, which was calculated by the formula: (total soybean) + (total meat). h Net means net realization per ha, which was calculated by the formula: (gross evaluation − cost per ha).

therefore, mechanized harvesting was not a problem. Pacheco et al. (2008) also observed that sowing palisade grass into R7-stage soybean (early defoliation at physiological maturity) had no effect on the mechanical harvesting of the soybean crop. The palisade grass treatments did not influence soybean yield components and seed yield. Notably, we expected that earlier intercropping (at the time of soybean sowing) may impair soybean development and reduce seed yield. According to Silva et al. (2009), the simultaneous sowing of palisade grass with soybean has a marked effect on both the soybean and the grass forage yield. With our results, we can infer that simultaneous intercropping of the soybean cultivar Embrapa 48 with palisade grass did not affect the seed yield of the cash crop or its components. Therefore, these results indicate that the appropriate time to sow palisade grass when intercropping will depend on the amount of grass forage desired, as it is likely that palisade grass sown earlier (on the soybean sowing date) will produce a higher quantity of dry matter. Note there was no difference between sowing on the soybean and 30 DAE, so if there is a need for a high quantity of grass straw, then intercropping could be within the first 30 d.

Soybean seed yields for both years were similar to those suggested by Embrapa Soja (2006) in the same cultivation system. Plant population, the number of seeds per plant and weight of 100 seeds were also similar between the years. Therefore, the larger number of pods per plant (38 in 2006–2007 and 27.4 in 2005–2006) likely elevated the seed yield in 2006–2007. This demonstrates the importance of this attribute with regard to crop yield, even when other attributes are not affected. Our success with sowing tropical forage with soybean and having no adverse effects on the cash crop yield can be attributed to several possibilities. First, although palisade grass has been reported to exhibit an allelopathic effect on soybean (Souza et al., 2006), this grass did not affect soybean seed yield. Second, planting palisade grass seeds at a depth of 8 cm reduced the emergence speed of the grass seedlings. When soybean and palisade grass were simultaneously intercropped, seedling emergence occurred at 6 and 13 d after sowing, respectively. Thus, the soybean emergence was more rapid than palisade grass, which likely allows soybean plant development without plant competition until about 50 DAE of soybean, similar results were observed by Kluthcouski

Table 7 Relative crop yield (RCY) and relative nitrogen yield (RNY) of soybean and palisade grass intercropped in two growing seasons. Treatments

RCY

RNY

Soybean (%)

Palisade grass (%)

Total (%)

Soybean (%)

Palisade grass (%)

Total (%)

Crop systems Simultaneously Oversowing – 30 DAE Oversowing R6

94.1 aB 94.8 a 99.7 a

42.9 b 47.9 a 48.7 a

137.0 b 142.7 ab 148.4 a

97.2 a 97.4 a 97.5 a

48.3 b 53.1 a 55.4 a

145.5 b 150.5 a 152.9 a

Growing seasons 05–06 06–07

98.7 a 93.6 a

43.8 a 46.9 a

142.5 a 140.5 a

95.6 a 99.1 a

49.9 b 56.6 a

145.5 b 155.7 a

A

A Simultaneously: palisade grass was sown simultaneously with soybeans; oversowing: palisade grass was oversown 30 d after the emergence (DAE) of soybeans; oversowing R6: palisade grass was oversown at the soybean reproductive stage R6 (full seed). B Values followed by the same lowercase letter, presented vertically, are not significantly different at p ≤ 0.10 according to Tukey’s test.

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et al. (2003). At this stage, competition could affect only seed filling and final seed weight; however we did not observe any of these effects. Third, our site (Botucatu in the State of Sao Paulo) exhibited low temperatures that could reduce the growth of the tropical forage and allow intercropping without the need for sub-lethal doses of herbicide. Fourth, the use of a cultivar with a shorter season length reduced the mutual competition. According to Crusciol et al. (2010), the season length duration of the soybean cultivar has a marked effect, and only early-cycle soybeans were successfully intercropped. They added that intercropping palisade grass with extremely early or early soybean cultivars is a viable option for crop–livestock integration because these conditions did not affect either soybean or palisade grass yield. Therefore, these cultivars could produce seeds and subsequently allow cattle to graze in the same area, providing greater revenue in comparison to a soybean monoculture or intercropping with longer-cycle cultivars. Fifth, palisade grass exhibits a slow initial development during the first month (Portes et al., 2000; Valle and Pagliarini, 2009). Forage plants can grow slowly because of sunlight interception by the soybean canopy. Sixth, when soybean was harvested, palisade grass exhibited only tender leaves, which were cut 5 cm above the soil surface and did not interfere with the harvest machinery. When palisade grass was intercropped with soybean, as observed the grass height at the time of soybean harvesting was similar to the soybean plant height. After this harvest, because the forage root system was already well established, the forage could grow without soybean competition, which allowed the palisade grass to accumulate dry mass. Seventh, the palisade grass seeding density (400,000 seeds ha−1 ) provided a palisade grass population of fewer than 8 plants m−2 at the time of the soybean harvest. Starting at a density of approximately 9 palisade grass plants m−2 , even when growth was controlled, the soybean seed yield was affected (Kluthcouski et al., 2003).

4.4. Forage dry matter production and crude protein After soybean harvest, the forage was cut 20 cm above the soil surface. However, the forage root system was already well established and, without soybean competition, the palisade grass was able to accumulate dry mass (Table 5). According to Portes et al. (2000), cash crops significantly affect palisade grass development, and, after cash crop harvesting, the forage develops rapidly and produces a similar biomass to that of a palisade grass monoculture after 60–70 d. The highest amount of PDMF in the earliest intercropping is due to the use of an early season cultivar (Embrapa 48), which, in addition to providing the highest soybean yields, favored the full development of palisade grass that is similar to what was reported by Crusciol et al. (2010). We observed an opposite response when palisade grass was sown at the soybean reproductive stage R6 (full seed) (4.6 Mg ha−1 ), where the grass was not fully established. For example, when palisade grass was sown earlier (simultaneously with soybean or at 30 DAE of soybean), the palisade grass was fully established after the soybean harvest. Moreover, in mid-April (autumn), the rainfall (58 mm in the first year and 110 mm in the second year) and temperatures (23 ◦ C in the first year and 22 ◦ C in the second year) allowed this grass to accumulate dry mass (Table 4). However, the low temperatures in June and July (16 and 15 ◦ C, in the first year, and 17 and 18 ◦ C, in the second year) and the decreased photoperiod limited the growth of palisade grass sown at the soybean reproductive stage R6 (full seed) (Muller et al., 2002)

because it was not as well-established as palisade grass that was sown earlier (simultaneously with soybean or at 30 DAE of soybean). At the 2nd cut in October, there were no differences in the forage dry matter production among all cropping systems. The onset of spring, marked by regular rains, increasing temperatures and a proper photoperiod, provided favorable conditions for the returning grass growth (Fig. 1). Therefore, independent of the palisade grass seeding date, these forage crops were already wellestablished at the 2nd cut and expressed their growth potential (Table 4). According to Costa et al. (2005), palisade grass develops optimally between 30 ◦ C and 35 ◦ C and does not grow at temperatures between 10 ◦ C and 15 ◦ C. These authors reported that low rainfall, characteristic of regions with a dry winter like the Cerrado region in Brazil during June and July, also attributes to the reduced palisade grass development (production of leaves and tillers). We also observed a reduction in development in our experiments, where intercropping performed later allowed less time for palisade grass development, similar to what occurs during poor climatic conditions, evidenced by differences in the dry matter accumulation. Notably, a satisfactory amount of palisade grass was produced in all treatments in both cuts, where dry matter production was higher than 4.0 Mg ha−1 . In addition, the 2-year average of the sum of the two cuts for palisade grass simultaneously sown with soybean, palisade grass sown 30 DAE of soybean and palisade grass sown at the soybean reproductive stage R6 (full seed) was 18.9, 18.5 and 14.2 Mg ha−1 of forage dry matter, respectively, at the time of the greatest forage demand for animals (winter/spring). These observations are important for the Cerrado and other regions, such as the African Savannas, where the autumn/winter season is dry with low temperatures and little precipitation; consequently, forage development and biomass production are limited (Kluthcouski et al., 2003; Costa et al., 2005). The biomass produced by palisade grass in our experiment could be used for cattle grazing without weight loss. Given that none of the treatments influenced the soybean yield, our results suggest that sowing palisade grass at the soybean reproductive stage R6 (full seed) is the least viable option to produce the most palisade grass dry matter. Regarding crude protein concentration in palisade grass leaves, the recorded values ranged from 107 to 139 g kg−1 of crude protein and were higher than the 70 g kg−1 , which is considered by Van Soest (1994) to be the minimum amount necessary to maintain a microorganism population in the rumen of cattle. Despite the lack of a N measurement from the soil, soybeans may have provided some N to the palisade grass, which may have contributed to increases in dry matter production and protein concentrations. According to Filizadeh et al. (2007), grass crop yields increase when the grasses are cultivated after soybean, which they attributed to an increase in N availability in this environment. Even without a precise measurement of the amount of N supplied from the soybean fixation to palisade grass, the forage did not display nitrogen deficiency symptoms, and these results were obtained without any supplementary fertilization. Additionally, the pasture can be recovered at a smaller cost because the same operation can sow the crop and palisade grass and apply fertilizer, as was performed in this study. New palisade grass seeds, cash crop fertilizer and soil liming contribute to vigorous plant and root development by this forage, which allows for year-long soil cover and the cycling of nutrients, increases levels of soil organic matter and soil water retention, reduces soil temperature oscillations, increases soil biological activities, and reduces weed growth and, consequently, herbicide use (Kluthcouski et al., 2003; Borghi and Crusciol, 2007; Garcia et al., 2008; Crusciol and Soratto, 2007, 2009; Crusciol et al., 2010,).

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4.5. Economic evaluations It was observed that simultaneous intercropping of soybean and palisade grass resulted in 1.6 times more revenue than soybean alone. This is because intercropping did not affect the soybean seed yield and because farmers can use the forage dry matter for animal fodder. Our data indicate that intercropping soybean with perennial forage plants is a great option for farmers, especially in tropical regions of South America, Africa, and parts of Asia where people need opportunities to produce food. In addition, we could include Oceania, especially Australia, because it has a suitable climate for developing this new crop system. Crusciol et al. (2010) demonstrated a 60% increase in revenue achieved by intercropping soybeans and palisade grass, compared with soybeans alone. Tedla et al. (1999), Reda et al. (2005), Rufino et al. (2006), Sulc and Tracy (2007), Tracy and Zhang (2008), Maughan et al. (2009), Crusciol et al. (2010), Nascente et al. (2013b) and Borghi et al. (2013) have all demonstrated that crop–livestock integration produces better results than cash crops sown alone. These authors have reported increases in cash crop yield, straw on the soil surface, nutrient cycling, and soil organic matter, erosion reduction and increased revenue. 4.6. Relative crop and nitrogen yield Regardless of the treatments, it was observed that intercropping soybean with forage species provided increases in the total relative crop yield (RCY) and total relative nitrogen yield (RNY). Besides, relative crop yields from intercrops were higher than the monoculture species cultivation. Soybean may have produced N taken up by grass, which could be observed in the intercrops treatments (Table 7). Therefore, the intercrops treatments allow increasing the total RCY and RNY per area. Then, we could infer that these intercropping systems (soybean + palisade grass) could provide many advantages, such as increasing nutrient cycling (N) like reported by Rufino et al. (2006) and Nascente et al. (2013a). However, we could see also that the intercrop simultaneously reduced both RCY and RNY in relation to the others intercrops, which could be because the greater time of competition between the two crops. Crusciol et al. (2010) showed that when increasing the time to live together in the intercrop reduced the both crop yield, corn and palisade grass dry matter. 5. Conclusions Summarizing, intercropping soybean and palisade grass is a good option for diversifying activities on farms and maximizing soil use throughout the year. Most farmers in Brazil produce only one crop during the growing season (Kluthcouski et al., 2003). However, with crop–livestock integration, seeds can be produced and cattle can graze in the same area afterward, which increases revenue per area. Crusciol et al. (2010) observed that soybean cultivars with a shorter season intercropped with palisade grass did not affect the soybean yield. They added that animals grazed for an additional 200 d after the soybean harvest, resulting in a 60% larger revenue compared with a soybean monoculture. Additionally, Rufino et al. (2006), Borghi and Crusciol (2007) and Tracy and Zhang (2008) demonstrated better results with agriculture–livestock integration compared with a crop monoculture. Crop–livestock integration may allow for the production of more food in the same area while benefiting the environment and increasing profits, which may allow farmers to diversify activities without expanding the agricultural area. Our results suggest that sowing soybean with palisade grass at all the times evaluated did not significantly affect either soybean nutrition or seed yield.

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Conversely, sowing palisade grass at the soybean reproductive stage R6 (full seed) significantly reduced the forage yield.

Acknowledgments To the São Paulo Research Foundation (FAPESP) for financial support (Registry number: 2003/09914-3), and to the National Council for Scientific and Technological Development (CNPq) for an award for excellence in research of the first author.

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