Concentrations and uptake of micronutrients by oat and pea in intercrops in response to N fertilization and sowing ratio

In intercropping systems, two or more crops are cultivated in such a way that they interact agronomically (Vandermeer, 1989). Benefits of intercropping are widely reported for grain yield and grain N yield. In pea–barley intercrop experiments conducted across Europe, grain N yield advantages of 25–30% were found compared to the respective sole crops (Hauggaard-Nielsen et al., 2009). In oat–pea intercrops grown in eastern Austria, no grain yield advantage was noticeable but a grain N yield advantage in unfertilized treatments could be observed because of the higher grain N concentrations of oat in intercrops (Neugschwandtner and Kaul, 2014, 2015). Oat–pea intercropping resulted in higher grain nutrient yields of macronutrients potassium (K), magnesium (Mg), and phosphorus (P) in N-unfertilized treatments and in higher residue macronutrients yields of calcium, K, Mg, and P over several N treatments compared to oat and pea pure stands (Neugschwandtner and Kaul, 2016).

Little consideration has been paid yet to micronutrient status of plants in intercrops, although intercropping could be an effective and a sustainable pathway for biofortification (of Fe and Zn) (Zuo and Zhang, 2009). Biofortification is the process of enriching nutrient concentrations of crops during growth (Jeong and Guerinot, 2008). Approaches for increasing micronutrient concentrations in food range from plant breeding to agronomic measures, for example, organic or inorganic fertilization, cultivar selection, or crop rotation (Rengel et al., 1999; Cakmak, 2008). Additionally, intercropping could facilitate micronutrient management because of the soil–plant–microbial interactions in the rhizosphere, which influence micronutrient availability (Watson et al., 2012). In multispecies ecosystems, the use of a resource (e.g., a nutrient) by plants may be characterized either by competition (for the same resource pool), complementarity (resource partitioning between intercrops through a differentiated use in time, space, and forms) (Fridley, 2001), or facilitation (one plant enhances the survival, resource availability, growth, or fitness of the other) (Callaway, 1995). For example, in wheat–chickpea intercrops, N, P, K, and Fe concentrations in wheat grain and Mn and Zn concentrations in chickpea grain increased compared to pure stands (Gunes et al., 2007).

Crop mixtures are extensively grown in traditional agricultural systems of developing countries (Biabani, 2009), and yield advantages have been reported for low soil fertility or low N fertilizer input systems (Bedoussac and Justes, 2011; Neugschwandtner and Kaul, 2014, 2015). Consequently, the focus of intercropping research on small-scale resource-poor systems has caused a knowledge gap in regards to high-input intercrop systems, which detracts from their rapid spread (Midmore, 1993), although there is an increasing interest in temperate regions for developing sustainable farming systems (Aufhammer et al., 2004; Kübler et al., 2008; Zając et al., 2014).

Therefore, the aim of this study was to assess oat–pea intercrops grown on a fertile soil in temperate conditions of eastern Austria as affected by N fertilization and sowing ratio with focus on (a) micronutrient concentrations of grain and residue, (b) uptake of micronutrients in grain and residue, and (c) nutrient harvest indices of intercrops as compared to pure stands of both crops.

Micronutrient concentrations in grain and residue varied between the cooler and wetter year 2010 and the drier and hotter year 2011. Nutrient concentrations and nutrient uptake in crops are reported to be reduced by drought because of its effects on root growth, lower nutrient mobility in the soil, and reduced transpiration flow (Fageria et al., 2002; Gunes et al., 2006). Accordingly, concentrations of all four analyzed micronutrients in the residue of both crops and Cu, Mn, and Zn in pea grain were generally considerably higher in 2010 than in 2011. Contrary to that, Cu, Fe, and Mn were lower in oat grain in 2010 than in 2011. Also Neugschwandtner et al. (2015a) have reported higher concentrations of Cu and Zn in grain and residue of pea under conditions of drought.

Diverse results have been reported for the influence of N fertilization on micronutrient concentrations. Similar to our results with higher Cu and Zn concentrations (and no alterations of Fe and Mg) in grain of oat and pea with N fertilization, Shi et al. (2010) reported higher concentrations of Cu, Fe, and Zn (but not of Mn) with N fertilization for wheat. They further observed that the proportions of elements were different between milling fractions attributing this to different pathways for the translocation and accumulation of individual micronutrients to the grain that are influenced by N. Also Ciampitti and Vyn (2013) reported higher Cu, Fe, and Mn concentrations with N fertilization for maize grain in pure stands. Contrary to that, no effect of N fertilization on concentrations of Fe and Zn in grain of winter wheat and spring barley was observed by Sedlář et al. (2014) and on micronutrient concentrations in grain of maize by Lošák et al. (2011). Ahmadi et al. (1993) observed even lower concentrations of Cu, Zn, and Mn with N fertilization in oat grain, attributing this to a dilution because of a higher grain yield.

Nutrient concentrations in pea were more affected by intercropping compared to oat. Oat grain had similar concentrations in all treatments, whereas pea grain had higher micronutrient concentrations in intercrops with a lower pea share in one year. Concentrations in residues were higher for Cu and Fe with lower oat shares but for all four elements in pea residues in some intercrops. Micronutrient concentrations of legumes in grass–legume mixtures grown in Denmark with different N regimes were found to be relatively constant between pure stands and mixtures but the concentrations in grasses were increased (Høgh-Jensen and Søegaard, 2012). A reason for differences in nutrient concentrations because of different plant densities (in which each component species in the substitutive intercrops occurred) can be concentration or dilution processes. For example, the grain N concentrations in pure wheat stands with higher seeding rate can be lower (at higher thousand-kernel weight (TKW)) (Arduini et al., 2006) or higher (at lower TKW) (Dai et al., 2013), whereas no influence of plant density was reported for Cu, Fe, Mn, and Zn in grain of maize pure stands (Ciampitti and Vyn, 2013). Further on, facilitation mechanisms between gramineous species and dicots for the uptake of nutrients have been reported by Zhang et al. (2010) (for Fe and Zn). For example, the release of root exudes (citric acid) in the rhizosphere of white lupin in an alkaline soil caused acidification and subsequent release of P as well as Cu, Fe, Mn, and Zn (Gardner et al., 1983; Dinkelaker et al., 1989). Consequently, a facilitation of the mineral nutrition of wheat and chickpea in intercrops has been reported with higher grain concentrations of N, P, K, and Fe in wheat and Mn and Zn in chickpea and higher shoot concentrations of P, K, Fe, Mn, and Zn in wheat and Mn and Zn in chickpea (whereas N, P, and K decreased in chickpea shoots) (Gunes et al., 2007). The positive influence of accompanying plants has also been shown in strip intercropping experiments: a higher concentration of Cu and Fe was observed for maize biomass placed next to bean compared to maize in the centre of the strip that was more distant to bean (but for which a higher Mn concentration was reported) (Głowacka, 2013). Similar to our results, Li et al. (2004) observed in wheat–chickpea intercrops higher Zn concentrations in the shoots of both the crops and higher Mn concentrations in the shoots of chickpea.

Differing results have been reported for Fe concentrations in cereal–legume intercrops. Our results showed just effects on pea grain and residue in one year. An enhancement of Fe concentrations has also been observed for peanut leaves intercropped with maize (Zuo et al., 2000), maize intercropped with bean (Głowacka, 2013), and for both species in wheat–chickpea intercrops (Gunes et al., 2007). In an Fe-deficient calcareous sandy soil, Cu, Fe, and Zn concentrations and chlorophyll content of peanut shoots intercropped with gramineous species (barley, oat, maize, or wheat) were much higher than those in mono-cropped peanut (Zuo and Zhang, 2008). Two reasons are given for that observation: dicot plants such as peanut and pea increase reductase activity under Fe deficiency and the release of protons and reductants is enhanced from the roots to mobilize Fe from the rhizosphere (Schmidt, 2003; Zuo and Zhang, 2008). On the other hand, gramineous plants exudate phytosiderophores into the rhizosphere under Fe and Zn deficiency to increase the availability of Fe and Zn (Marschner et al., 1998; Schmidt, 2003). The release of phytosiderophores by maize was also found to increase the Zn nutrition of an accompanying peanut crop (Inal et al., 2007). For Fe and Mn, there are antagonistic reactions in the uptake of these elements in plants (Tanaka and Navasero, 1966). Consequently, higher Fe but lower Mn concentrations have been observed in intercrops for maize strip cropped with bean (Głowacka, 2013), whereas in maize–peanut intercrops, the shoot concentrations of Fe were increased in peanut but Mn in peanut shoots and Fe and Mn in maize shoots were not affected (Inal et al., 2007). We observed no changes for Mn in grain and residue of oat but higher values in intercropped pea in one year for both Fe and Mn. Lošák et al. (2011) also stated that Fe did not inhibit the uptake of Mn in maize grain. Uptake of Cu, Mn, and Zn in grain and Cu, Fe, Mn, and Zn in residue of oat increased with N fertilization through both higher concentrations of these elements and a higher biomass production with N fertilization. While no higher uptake with N fertilization was observed for pea grain, the higher uptake of Cu and Zn in pea residues was caused by higher element concentrations with N fertilization. Lower nutrient harvest indices of oat for Fe and Mn and of pea for Cu, Fe, Mn, and Zn indicate that nutrient uptake efficiency was more enhanced than nutrient utilization efficiency with N fertilization (cf. Neugschwandtner et al., 2015b).

Crop-specific uptake of micronutrients by grain and residue of oat and pea decreased with lower share for each crop with a lower decrease for the dominant crop oat than for pea. The total grain LER_Nutr was clearly above unity only for Mn and Zn in unfertilized 75%:25% and 50%:50% oat– pea intercrops (except for Mn in the 75%:25% intercrop in 2010). Consequently, a grain nutrient yield advantage by intercropping oat and pea could just be obtained in these intercrops compared to pure oat and pea stands. On the other side, the total residue LER_Nutr was partly considerably above unity, indicating a high nutrient yield advantage in residue of oat–pea intercrops at each sowing ratio compared to pure stands. The contribution of oat to the total grain and residue LER_Nutr was considerably higher than that of pea as considerably higher partial LER_Nutr of oat than of pea at equal sowing ratios of each crop show. Values of the total grain LER_Nutr were generally in a similar range as the total grain LER as just the grain concentrations of pea (which was not as strongly represented as oat in the intercrops) were partly increased in the intercrops. The total residue LER_Nutr, however, was generally higher than the total residue LER as for both crops statistically confirmed or at least tendencies of higher nutrient concentrations in intercrops were observed.

The nutrient harvest index especially of oat and partly of pea decreased with a lower share of the crops in the intercrops, indicating that the nutrient utilization efficiency was lower in intercrops than in pure stands.

Micronutrients (including Cu, Fe, Mn, and Zn) are required for ruminant feeding especially as central elements of enzymes. Deficiencies can negatively affect growth and fertility (Hidiroglou 1979; Fischer, 2008). Ideally, mineral nutrition requirements of livestock should be covered by a judicious combination of natural feeds (e.g., by adding protein concentrates to a grain mixture). Additionally, mineral supplements are used to meet requirements (Suttle, 2010). For example, supplementation of dairy cow diets with Cu, Mn, Zn, and cobalt reduced days to first estrus (Campbell et al., 1999) and increased milk production (Yamamoto et al., 2014). The body weight gain of crossbred male calves was shown to increase with the supplementation of Cu, Fe, Mn, and Zn (Mondal et al., 2009).

Micek et al. (2012) have reported that intercropping resulted in a higher protein yield and a higher nutritive value of harvested grains for food and feed. Additionally, crop residues are an important feed resource for ruminants (especially in developing countries) (Zerbini and Thomas, 2003). Feeding residues may constitute a major part of the maintenance ration for wintering mature, dry, pregnant beef cows but is not recommended for feedlot cattle (Anderson, 1978). However, residues are often severely deficient in one or more major nutrients required by ruminants (including protein, vitamins, and minerals) (Coleman and Moore, 2003), and detailed nutritional analysis of residues is often not available (McCartney et al., 2006). Consequently, quality-improved residues could help to meet additional feed demands of ruminants, which arise owing to the increasing demand for livestock products (Bartle and Klopfenstein, 1988).

In oat–pea intercrops grown on a fertile soil in eastern Austria, higher micronutrient grain yields could just be obtained for Mn and Zn in unfertilized intercrops with a medium to high oat share, whereas the micronutrient residue yields of the intercrops surpassed those of the pure stands of both crops. This indicates that possible benefits for obtaining higher micronutrient yields with intercrops for producing grain feed are limited to a low N input level, whereas higher micronutrient residue yields are achievable over all intercropping ratios and fertilization levels. Thus, intercropping can be a strategy for increasing micronutrient yield in residue that can be used for ruminant feeding.