Attribution of crop yield responses to application of organic amendments: A critical review

Soil & Tillage Research 186 (2019) 135–145

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Review

Attribution of crop yield responses to application of organic amendments: A critical review

T

Corinne Celestinaa,b,c, , James R. Huntb,c, Peter W.G. Salec, Ashley E. Franksa,b ⁎

a

Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, 3086, Australia Centre for Future Landscapes, La Trobe University, Bundoora, VIC, 3086, Australia c Department of Animal, Plant and Soil Sciences, AgriBio the Centre for AgriBiosciences, La Trobe University, Bundoora, VIC, 3086, Australia b

ARTICLE INFO

ABSTRACT

Keywords: Organic matter Fertilizer Soil Nitrogen Experimental design

Soil organic matter affects soil physical, chemical and biological properties and is thus agronomically important because these factors affect crop yields. Organic amendments such as manures, composts and plant residues are frequently used in crop production systems as alternatives to inorganic fertilizers, to restore degraded soils and ameliorate physicochemical constraints. Crop yield responses to the application of organic amendments can be due to the amelioration of soil constraints, plant nutrients contained in the amendment, or both factors acting in concert. Because of the way in which many organic amendment experiments are conducted, these factors can be confounded due to poor experimental design leading to difficulties in accurately ascribing crop yield responses to these different factors. In this review we consider three scenarios where organic amendments are used as fertilizers, soil restorative agents and soil ameliorants to highlight common limitations of these experiments that prevent attribution of crop yield response. To overcome these limitations, we provide guidelines for the design, conduct and analysis of organic amendment experiments which will allow the attribution of yield responses to nutrition, alleviation of physicochemical constraints, or other factors. To achieve these aims, field experiments must (1) identify a genuine constraint to crop yield at the experimental site; (2) incorporate proper treatments to control for the effects of nutrient content and method of placement; (3) use appropriate sampling protocols to assess treatment differences; (4) carry out suitable soil and plant analyses; and (5) be conducted over several sites and years. Controlled environment experiments and modelling approaches may also be used to overcome some of the limitations of field experiments and provide a detailed mechanistic understanding of the crop yield response.

1. Introduction

associated organic matter – that differ based on their chemistry, origin and stability over time (Kögel-Knabner and Rumpel, 2018; von Lützow et al., 2007). Whilst soil organic matter contains around 50% carbon (C) (Pribyl, 2010), it also contains high levels of nitrogen (N), phosphorous (P) and sulfur (S) in fixed ratios (Kirkby et al., 2011) that are released to the plant as they mineralize. This CNPS stoichiometry has implications for building soil organic matter: every unit increase in C requires a fixed input of N, P and S (Kirkby et al., 2013). Increasing soil organic matter content can be achieved by the application of organic amendments, which contain C and other nutrients, or by the addition of inorganic fertilizers and a source of C such as in crop residues (Alvarez, 2005). Organic amendments have been applied to soils in order to restore or maintain soil fertility, structure and productive capacity since the beginning of agriculture (Churchman and Landa, 2014). Maintaining or increasing organic matter via these methods is expected to

Soil organic matter is a critical component of productive soils. It influences a wide range of physical, chemical and biological attributes and processes, including the formation and stabilization of soil aggregates, nutrient cycling, water retention, disease suppression, pH buffering and cation exchange capacity (Loveland and Webb, 2003; Murphy, 2015). Consequently, organic matter is important from an agronomic perspective because it has the potential to influence crop yields via any of these processes (Oelofse et al., 2015). Soil organic matter is a complex mixture of organic compounds such as plant residues, microbial products and rhizosphere inputs in various stages of decomposition (Kögel-Knabner and Rumpel, 2018; Lehmann and Kleber, 2015). It can be divided into several functionally relevant pools – e.g. free or occluded particulate organic matter, mineral-

⁎ Corresponding author at: Department of Animal, Plant and Soil Sciences, AgriBio the Centre for AgriBiosciences, La Trobe University, Bundoora, VIC, 3086, Australia. E-mail address: [email protected] (C. Celestina).

https://doi.org/10.1016/j.still.2018.10.002 Received 3 July 2018; Received in revised form 14 September 2018; Accepted 2 October 2018 0167-1987/ © 2018 Elsevier B.V. All rights reserved.

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maintain or increase crop production, whereas decreasing organic matter is implicated in declining yields (Lal, 2006; Loveland and Webb, 2003). In recent years, our understanding of the organic matter-crop productivity relationship has been tested, with several studies challenging the relative contribution of soil carbon, organic matter or organic amendments in contributing to crop yields. These meta-analyses of long-term experiments have highlighted the need to separate the ‘organic matter effect’ from other confounding variables, such as improved plant nutrition (Dawe et al., 2003; Edmeades, 2003; Oelofse et al., 2015; Schjønning et al., 2018). In terms of organic amendments, the nutrient contained within the amendment and the associated fertilizer response on the crop is frequently overlooked, and it is often impossible to separate this fertilizer effect from the effect of the organic matter itself due to confounded experimental design (Dawe et al., 2003; Hijbeek et al., 2017; Oelofse et al., 2015; Schjønning et al., 2018). Schjønning et al. (2018) have called for a renewed conceptual understanding of the role of organic matter in crop production, with an emphasis on separating the nutrient (N) and non-nutrient effects of organic matter on yield using properly designed experiments. This same consideration needs to be made for experiments testing the effects of organic amendments on crop production. It is critical to be able to accurately attribute crop yield increases resulting from the addition of organic amendments if we are to understand the drivers and mechanisms underlying crop productivity. It is not the intention of this review to devalue the importance of soil organic matter to productive managed ecosystems, nor to promote the wholesale abandonment of organic amendments in favor of inorganic fertilizers. It is important to recognize that soil organic matter and soil carbon have many direct and indirect benefits to the soil system and the environment beyond their impacts on crop productivity; likewise, there are issues to consider around the sustainable long-term use of inorganic fertilizers (for reviews see Diacono and Montemurro, 2010; Larney and Angers, 2012; Powlson et al., 2011). Instead, the aim of this review is to demonstrate that there are multiple factors that contribute to crop yield responses to organic amendments, and that properly designed and monitored experiments need to be conducted in order to accurately ascribe these yield responses to a change in soil physicochemical properties or some other factor such as increased nutrient supply. Scenarios involving three uses of organic amendments – as alternatives to inorganic fertilizers, for the reclamation of degraded soils, and to ameliorate subsoil constraints – are used to highlight common limitations in field experiments that prevent the accurate attribution of yield. We conclude with a list of guidelines for the design and evaluation of organic amendment experiments that allow attribution of yield responses.

2006). These changes can ultimately lead to an increase in crop yields (Diacono and Montemurro, 2010; Lal, 2006). However, organic amendments can also provide significant nutrients to the plant in mineral form, which directly improve crop yields via fertilization. It is often difficult to separate fertilization from other effects of the organic amendment on crop yield due to the experimental design used. Experiments on the use of organic amendments frequently report significant increases in crop yield and improvement in soil properties in comparison to a ‘district practice,’ un-amended or reduced-nutrient control (Agbede and Ojeniyi, 2009; Barzegar et al., 2002; Cherif et al., 2009; Courtney and Mullen, 2008; Zhang et al., 2000). The rates of organic amendments applied in field experiments deliver rates of nutrients that are in the linear section of nutrient response curves. For this reason, the ‘best’ rate of organic amendment frequently matches with the highest rate applied and inevitably also corresponds to the greatest amount of nutrients supplied. Thus, the crop response may be due to the fertilizer effect of the amendment, some effect related to the carbon or biological components of the amendment, or a combination of both. Because there is no treatment to control for the high rates of nutrients supplied by the amendment, then it is not possible to determine why the yield response occurred as causes are confounded. Where the total nutrient content of the organic amendments and inorganic fertilizers are matched (or approximately equivalent), crop yields are often comparable (Mantovi et al., 2005; Montemurro, 2009; Nyakatawa and Reddy, 2000a; Zhang et al., 2000) regardless of the method of application used (e.g. surface broadcasting, liquid injection, subsurface banding) (Celestina et al., 2018; Sistani et al., 2017). In these studies cited above, N was the nutrient matched across treatments, demonstrating that where total N supply was matched, yields of organic amendment and synthetic fertilizer treatments were the same. Several independent meta-analyses of long-term experiments worldwide have concluded that organic amendments and inorganic fertilizers have similar effects on crop yields when they are applied at equivalent rates of macronutrients (N, P and K), with organic amendments not conferring any additional advantage over and above that derived from the application of nutrients in fertilizer (Edmeades, 2003; Hijbeek et al., 2017). By controlling confounding variables and comparing treatments with equivalent nutrition applied over a period of 5–120 years, these meta-analyses concluded that although organic amendment-treated soils frequently had higher organic matter content, enhanced microbial activity and better soil structure, the crop yields of organic amendment treatments were equivalent to those of matched inorganic fertilizer treatments (Chen et al., 2018; Dawe et al., 2003; Edmeades, 2003; Hijbeek et al., 2017; Oelofse et al., 2015). Such longterm experiments are necessary to identify the impact of organic amendments on crop yields because they may have cumulative effects that are not immediately evident in the short-term (Abbott et al., 2018; Diacono and Montemurro, 2010). Edmeades (2003) suggest that organic amendments may only have additional benefits to soil quality and productivity when they are applied annually at very high rates (> 35 t/ ha) over a very long period of time (> 100 years) – an economically infeasible solution. Thus, available data from long-term experiments do not provide much evidence that organic amendments provide a crop yield benefit compared to inorganic NPK fertilizers in situations where sufficient nutrients are supplied by the fertilizer (Dawe et al., 2003; Hijbeek et al., 2017). In terms of increasing crop yields, the indirect effect of organic amendments on crop productivity – e.g. via the effects on soil carbon, chemistry and structure – appear to be less important than the direct effect of increased nutrient supply on crop nutrition. Equivalent yields were often reported in nutrient-balanced organic and inorganic treatments, even when significant improvements in other soil parameters (e.g. carbon content, chemical fertility, soil structure) were measured in response to the addition of organic amendments only (Edmeades, 2003; Mantovi et al., 2005; Nyakatawa et al., 2001; Sistani et al., 2014). Regardless of amendment type, the nutrient-rich treatments frequently

2. Scenarios involving organic amendment experiments 2.1. Organic amendments as alternatives to inorganic fertilizers There are many reasons why it may be desirable to use organic amendments as an alternative to traditional synthetic fertilizers. An oftcited reason is to replenish depleted soil organic matter, and thus benefit from the physical, chemical and biological properties that are associated with high organic matter soils (Diacono and Montemurro, 2010; Loveland and Webb, 2003; Murphy, 2015). Additionally, organic amendments may be used to improve plant nutrient uptake, maximize nutrient-use efficiencies or reduce environmental impacts compared to inorganic fertilizers (Edmeades, 2003; Quilty and Cattle, 2011). In some agricultural systems, such as smallholder subsistence farming, animal manures are used as fertilizers as they are the only feasible and affordable sources of plant nutrients available in many instances (Onduru et al., 2008). Organic amendments can increase soil carbon and, by a series of interdependent processes, improve biological activity, soil structure, cation exchange, water holding capacity and so on (Lal, 136

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exhibit elevated concentrations of nutrients in plant tissues or grain proteins compared to untreated controls (Celestina et al., 2018; Erhart et al., 2005; Mantovi et al., 2005; Sistani et al., 2017, 2014), indicating a probable nutrient response to the amendments. However, without the necessary treatments to control for the fertility supplied by the organic amendments, it is not possible to definitively attribute yield to either effect.

because of concerns regarding seasonal variation, nutrient toxicity and excessive costs (Dormaar et al., 1988; Smith et al., 2000). Whilst experimental evidence suggests the yield response may be due to a combination of fertilizer and soil restoration effects, appropriate experimental design and measurements of changes to both plant growth and soil physicochemical properties following the application of the amendments, are required to demonstrate this. Experimental results are further complicated by observations that increased crop yields do not always go hand-in-hand with improvements in soil physical properties (Larney et al., 2005). Furthermore, in most cases these experiments have failed to account for the indirect effects of the organic amendment on soil carbon, structure and biological fertility. The addition of an organic amendment rich in nutrients can increase soil organic matter directly, via the deposition, decomposition and stabilization of the amendment itself, and indirectly via increased below-ground biomass production and root exudation of a well-fertilized crop (Alvarez, 2005; Kirchmann et al., 2013). Increasing carbon inputs from roots and root exudates can in turn promote enhanced microbial activity and the formation and stabilization of aggregates, thus improving soil structure (Bronick and Lal, 2005; Six et al., 2004). Appropriate soil and plant analyses, controlled environment experiments and modelling approaches are required to untangle these complex mechanisms responsible for improvements in soil physical properties and yield responses.

2.2. Restoration and reclamation of degraded soils with organic amendments Soils that are degraded by natural or man-made processes such as mining, erosion or continuous cropping are typically low in organic matter and so many attempts to restore or reclaim these soils focus on additions of organic amendments (Larney and Angers, 2012). In this situation, it is anticipated that addition of organic amendments will restore the productive capacity of the degraded soil by increasing soil organic matter content and its attendant benefits (Lal, 2006). However, although studies on eroded soils have demonstrated that a reduction in soil organic matter is linked to reduced crop yields, addition of inorganic fertilizer has been shown to maintain yields very close to those of un-eroded sites (Loveland and Webb, 2003). As with the use of organic amendments as alternative fertilizers, in the case of soil restoration the role of nutrients in the crop yield response is often not separated from other soil physicochemical effects. Although many experiments provide clear evidence of improvement in soil physical and chemical properties – that is, evidence of restoration and reclamation of the degraded soil – the contribution of the nutrients in the amendment to increased crop yields was not accounted for in the experimental design. For example, higher crop yields on industrial sites in Alberta, Canada after topsoil replacement and organic matter addition were linked to increased soil organic carbon (Larney et al., 2005, 2003). However, the amendments used contained considerable nutrients: 139–880 kg ha−1 N and 9–225 kg ha−1 P (Larney et al., 2005, 2003). Whilst the authors measured positive changes in soil carbon and physical structure of the restored soil, a typically organic matter-rich Chernozem, they also measured increased soil N and P fertility after addition of amendments. This is not unexpected given that, in soil organic matter, C, N, P and S are stoichiometrically linked: a measured increase in soil organic carbon invariably means that there has also been an increase in these macronutrients in the organic matter (Kirkby et al., 2011; Tipping et al., 2016). Adeli et al. (2017) also reported significant yield improvements on eroded agricultural Luvisols in southeastern United States, with crop yields and N and P uptake increasing linearly with organic amendment application rate in comparison to an un-amended control treatment. Soil physical, chemical and biological properties including pH, bulk density and microbial biomass were also improved by the addition of organic amendment, relative to an unfertilized control (Adeli et al., 2017). Similarly, inorganic fertilizer additions were deemed less effective at restoring the productivity of eroded agricultural Chernozem soils in western Canada when compared to applications of manure with 8–16 times more N (Larney et al., 2000). Soil properties were not measured but authors did report increased concentrations of nutrients in the grain and credited the success of the manure to its ability to supply macro- and micronutrients to the crop long-term (Larney et al., 2000). The addition of N from inorganic fertilizer was also credited with restoring crop productivity on eroded soils treated with different amendments (Larney et al., 2003). In experiments such as these the omission of a matched-nutrient control means that it is difficult to definitively attribute the crop yield response to restoration of soil physical or chemical properties by the organic amendments, or simply to increased fertility due to the nutrients supplied by the amendments. Typically, high amendment rates were chosen to ensure productivity gains, not necessarily to be economical, and matched fertilizer nutrient treatments were not used

2.3. Deep incorporation of organic amendments to ameliorate subsoil constraints Organic amendments have also been applied directly to subsoils in attempts to improve soil properties deep in the profile. In the high rainfall zone of south eastern Australia, deep incorporation of organic amendments has been tested for its ability to ameliorate subsoil constraints to plant growth inherent in Solonetz soils which are associated with sodicity, high bulk density and poor physical structure. This process, termed subsoil manuring, has resulted in significant grain yield increases, relative to nil or low-nutrient application, for several years following the incorporation of high rates of nutrient-rich organic amendments such as poultry manure or lucerne pellets (Gill et al., 2012, 2008). These yield responses were attributed to the amelioration of subsoil constraints, increased water use and nutrient supply (Gill et al., 2012, 2009, 2008). A similar technique has been employed in the southeastern region of the United States, where subsoil compaction due to industrial or agricultural activities can constrain crop yields. Khalilian et al. (2002) reported that injected municipal solid waste increased crop yields, plant nutrient content, soil organic matter content and physical properties of a degraded Alisol, with the greatest results achieved with the highest rates of organic amendment. In another series of experiments, higher crop yields on Gleysol, Solonetz and Chernozem soils in southwestern Canada were attributed to soil structural improvement and higher nutrient availability (Leskiw et al., 2012; Leskiw and Zeleke, 2009). The basis of these results are complex because the improvement in soil structure and ensuing amelioration of subsoil constraints could be due to the placement of the organic amendment at depth, or to the nutrients contained in the amendment. The nutrient-rich amendments can directly stimulate plant growth by increasing soil fertility, thereby increasing soil water uptake and improving water use efficiency (Brown, 1971; Brueck, 2008; Gregory et al., 1984; Norton and Wachsmann, 2006). Similarly, the promotion of greater root growth and associated exudation and microbial activity can improve soil structure by encouraging the formation and stabilization of aggregates (Barto et al., 2010; Bronick and Lal, 2005; Six et al., 2004). As a case in point, Gill et al. (2009) reported a strong correlation between increased crop yield, root growth, extraction of subsoil water and soil physical properties after the subsoil incorporation of amendments. These observations could be due to the amelioration of subsoil constraints by the 137

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organic amendment, to improved nutrient supply and hence plant growth after addition of nutrient-rich amendments, or a combination of both. All of the studies cited above, with the exception of Khalilian et al. (2002), compared subsoil application of organic amendments to a deep tillage control or a ‘district practice’ control of no amendment and no tillage. The most successful organic amendments always contained very high rates of plant nutrients, particularly N and P. For instance, the Dynamic Lifter® (Yates, Australia) treatment used in the study of Gill et al. (2008) contained 800 kg ha−1 of total N and 440 kg ha−1 total P; the pelletized manure used by Leskiw et al. (2012) contained 360 kg ha−1 total N and 100 kg ha−1 total P. Given the large amounts of nutrients that were applied during addition of organic amendments, it is important to separate the likely yield increase due to this nutrition. If an increased supply of nutrients is able to explain the yield increase, then it may not be necessary to place the organic amendment in the subsoil, as a surface application of nutrients may suffice. Whilst authors in these studies measured positive changes in physical structure of the subsoil (Gill et al., 2009; Leskiw et al., 2012), they also measured greatly increased plant N uptake (Gill et al., 2012, 2008) and it is difficult to definitively attribute yield increase to either mechanism because there was no surface broadcast nutrient control. Some researchers investigating subsoil placement of amendments have included the appropriate experimental controls to separate these effects on yield. As with the scenarios discussed earlier, it is necessary to include a nutrient control treatment where an inorganic fertilizer supplies equivalent total nutrients in inorganic form as occur in the organic amendment. Additionally, because these experiments involve the deep incorporation of amendments to target constraints in the subsoil, it is essential to include a surface applied control where the same rate and types of amendments are applied to both the soil surface and the subsoil. These two experimental controls are necessary to (i) attribute yield increases to either a fertilizer effect or some carbon or biological effect of the amendment, and (ii) attribute yield increase to subsoil amelioration or mineral nutrition. Khalilian et al. (2002) included a surface broadcast amendment control in their 2002 study. More recent subsoil amelioration experiments carried out in Australia on a range of soil types also included a control treatment where organic amendments were applied to both the subsoil and the soil surface (Celestina et al., 2018; Hall et al., 2018). Of these experiments that included the surface applied amendment control, four site years showed a positive interaction between deep placement and amendment treatments implying that yield increases, due to deep incorporation of organic amendments may be due to more than nutrition alone. In terms of a matched nutrient control, Celestina et al. (2018) included this treatment to separate nutrient and non-nutrient effects in a series of field experiments using factorial combinations of amendment types (organic amendment, synthetic fertilizer) and placement methods (surface broadcast, deep tillage). Results from those experiments suggest that N fertility, not subsoil amelioration, may have been responsible for most of the crop yield response (positive, negative or negligible) to surface or subsoil placement of amendments (Celestina et al., 2018). Celestina et al. (2018) reasoned that crop yield responses to surface or subsoil placement of organic and inorganic amendments in these experiments were determined by the rules governing crop yield response to N fertilizer, whereby significant yield responses to N-rich amendments only occur in seasons where water-limited yield potential exceeds the yield limited by the existing N supply to the crop. Nevertheless, without detailed assessment of plant nutrient status and subsoil properties before and after treatment it is still not possible to conclusively ascribe plant yield increases to either subsoil amelioration, increased fertility or some other effect. Complementary approaches, such as the use of controlled environment experiments and simulation modelling, may also help to disentangle these effects.

3. Guidelines for the design and evaluation of organic amendment experiments 3.1. Identification of a constraint to crop yield at the field site Identification of a genuine and measurable constraint to crop yield is necessary before embarking on any soil amelioration or restoration practice. To do this, we recommend using a soil pit or intact cores to observe the soil profile and characterize the physical (e.g. bulk density, porosity, hydraulic conductivity), chemical (e.g. pH, salinity, sodicity, nutrient toxicity/deficiency) and biological (e.g. soil carbon, microbial activity) properties. A broad understanding of the complex way that these properties can interact to constrain crop roots is required. An example of a complex chemical constraint would be the impact of high pH (> 8.7 in water) and high sodicity, resulting in toxic concentrations of bicarbonate ions (Rengasamy, 2010). With respect to physical properties, an example would be the constraints posed by a dense clay subsoil with narrow least-limiting water range (Letey, 1985; da Silva et al., 1994), where roots can be constrained when soil is wet by poor aeration, and when dry by a strong soil matrix or low water availability (MacEwan et al., 2010). It is also essential when identifying constraints for soil physical and chemical measurements to be paired with observations of crop rooting depth and soil water uptake in order to determine whether the degraded soil or subsoil constraint is actually limiting plant growth and what the magnitude of the constraint might be. Thus, a plausible, explainable and measurable constraint to root growth must exist, and its impact on plant growth must be known, if yield increases from an amelioration intervention are to be explained and attributed to the alleviation of one or more constraints. Crop roots may be constrained in a degraded soil or in deeper subsoil layers by physicochemical means (e.g. salinity, sodicity, alkalinity, high bulk density), by an inadequate supply of nutrients, or a combination of both factors. The impact of these constraints, however, is complicated by the fact that plant roots are able to grow in some soils for which the properties are well outside the range of optimum values (Kaufmann et al., 2010). In some cases, crop roots can grow into a seemingly constrained subsoil through biopores (channels from earlier root growth) or through fissures between larger structural units (Passioura, 2002; Stirzaker et al., 1996; White and Kirkegaard, 2010). Only a low root length density is required for plant roots to extract moderate amounts of plant available water in a constrained soil (King et al., 2003; Kirkegaard et al., 2015) but the extraction of all of the subsoil water held above permanent wilting point (−1500 kPa) is generally incomplete due to root clumping and poor root-soil contact in biopores and decreasing root density and suction with increasing root length (Passioura, 2002, 1991). Incomplete use of plant available soil water by crops, often despite the presence of roots, has been reported by numerous authors (Kirkegaard et al., 2007; Robertson et al., 1993; Schultz, 1971). Notwithstanding the above scenarios, there are soils where the constraints are more severe. This is likely to occur in soils with severe chemical imbalances such as highly alkaline sodic subsoils, where root growth and water uptake cease completely, and crop yields are severely limited (Adcock et al., 2007; Dang et al., 2006; MacEwan et al., 2010). In order to provide evidence of a constrained soil, we recommended characterizing plant available water capacity using the method outlined by Burk and Dalgliesh (2013) whereby soil water extraction by an otherwise healthy crop (i.e. no nutrient limitations or other manageable abiotic or biotic stresses) growing on a constrained soil is assessed. This method is used to determine the crop lower limit (CLL, field measure of volumetric water content under a well-managed crop grown to maturity under terminal drought), drained upper limit (DUL, field measure of volumetric water content after drainage has ceased) and plant available water capacity (volumetric water content between DUL and CLL) of a given crop on a given soil (Burk and Dalgliesh, 2013; Dalgliesh et al., 2009). This procedure can be used to determine the severity of the soil 138

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Fig. 1. Representation of soil water profiles in an unconstrained soil (a) and in a constrained soil where root growth and water uptake is completely stopped (b) or restricted (c).

constraint as well as give an accurate assessment of how a particular soil management intervention might affect the crop’s ability to extract soil water from the root zone of the treated soil. In an unconstrained soil where root growth and soil water uptake are not constrained, CLL and DUL for a given crop will meet at the maximum rooting depth of that crop (e.g. at 2.0 m for the crop depicted in Fig. 1a). As noted above, in this scenario field measurements of CLL will naturally deviate from laboratory measures of permanent wilting point (−1500 kPa) at depth. On the other hand, if CLL and DUL meet at an unduly shallow depth (e.g. less than 1.4 m for wheat in SE Australia) it can be assumed that the plant has not extracted all available water from the profile and that a severe constraint to root growth exists (Fig. 1b). In this scenario depicted in Fig. 1b, CLL and DUL meet at a depth of 1.0 m, and root growth and soil water uptake are completely stopped at that depth. Less severe constraints to root growth and soil water extraction are demonstrated if CLL is substantially greater than laboratory measurements of permanent wilting point (Fig. 1c).

Table 1 Minimum amendment treatments required to separate effects on yield due to nutrition or other factors inherent to the organic amendment such as carbon content or biological activity.

uncertainties regarding the amounts and rates of nutrients released from organic amendments over time (for review see Schröder, 2005). Organic amendments can contain large amounts of macro- and micronutrients, a high proportion of which may only become available to plants over time as the amendment is mineralized (Quilty and Cattle, 2011). Different amendments also vary widely in their chemical composition and decomposition rate (Diacono and Montemurro, 2010; Flavel and Murphy, 2006), which makes matching the species and rates of all plant nutrients challenging. There are further difficulties with this comparison because high rates of nutrients can lead to toxicities (or induce deficiencies of other nutrients), or there may be losses of surface applied mineral nutrients to runoff, leaching and volatilization, particularly in high rainfall environments (Fillery and McInnes, 1992; Mathers et al., 2007). As a result, we recommend these inorganic fertilizer treatments use foliar applications, slow-release fertilizers (as per Sistani et al., 2014) or split applications (as per Mantovi et al., 2005) to ensure that nutrient supply matches demand throughout the growing season. In experiments where the amendment is applied at depth – whether to improve nutrient efficiencies in the case of subsurface banding or to ameliorate subsoil constraints in the case of subsoil manuring – it is critical that treatments are included that can differentiate the effects of nutrition from the effects of placement depth of amendment on crop yield. This is important because the most effective organic amendments often contain large amounts of nutrients, and so it is necessary to separate the likely yield increases due to nutrition alone if researchers are to attribute yield increases to plant nutrition, subsoil amelioration or

3.2. Appropriate experimental design for yield attribution When organic amendments are applied as alternatives to inorganic fertilizers it is critical that appropriate experimental controls are used to allow valid comparison of these treatments. That is, the same species and rates of key nutrients need to be provided to the plant by both the organic and inorganic fertilizer treatments to establish whether the organic amendment is providing a benefit to the crop over and above a direct fertilizer effect of nutrients. This is because the carbon and microbial components of organic amendments could increase crop yields for reasons other than nutrition – for example, by buffering soil pH and detoxifying aluminum, increasing soil aggregation or suppressing plant pathogens (Lehman et al., 2015; Murphy, 2015). Therefore, experimental treatments in which nutrients in the organic amendments are matched with inorganic fertilizers should be included to determine if a crop yield response to amendment is likely due to its nutrient content or some other process (Table 1). This approach requires analysis of the nutrient content of the organic amendment and an understanding of the availability of these nutrients to the plant over the course of the experiment. There are difficulties with this comparison, however, due to 139

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some other factor. Most importantly, a control treatment is required in which the same rate of amendment or matched fertilizer (and therefore nutrients) is applied to the soil surface. This surface-applied amendment may be incorporated by light cultivation or sowing operation as per district practice. Again, there are difficulties with this comparison because the tillage treatment can modify the effect of the amendment due to differences in soil properties and moisture content. Differences in pH, biological activity or clay mineralogy, for example, will result in differences in decomposition, mineralization and nutrient availability between the topsoil and subsoil (Rumpel and Kögel-Knabner, 2011). Tillage itself can also directly affect the availability of subsoil nutrients (Ozpinar, 2016; Schneider et al., 2017). In addition, placement of amendments above or below the soil surface, or in concentrated bands versus evenly spread, has implications for nutrient use efficiency and environmental losses (Pote et al., 2011; Rochette et al., 2013). Field experiments involving surface and subsoil application of amendments are inevitably going to be confounded by these differences to some degree. Therefore, in light of these limitations, the most appropriate design for a field experiment aiming to assess the impact of subsurface placement of organic amendments on crop yield is a balanced two-way factorial with ± deep tillage necessary for injection or incorporation and ± amendment treatments (Table 2). In such an experiment, yield response to subsurface placement can only be attributed to amelioration of subsoil constraints if there is a statistically significant interaction, with or without main effects, between amendment and deep tillage treatments (Fig. 2e–h). If there is no interaction between amendment and deep tillage treatments, yield response may be due solely to the amendment (Fig. 2b) or deep tillage (Fig. 2c) as main effects, or to a combination of the two (Fig. 2d). Alternatively, there may be no significant main effects or interaction and therefore no yield response (Fig. 2a). Finally, the complete set of treatments required to separate effects on crop yield due to nutrition or other factors in experiments where different amendments are placed on or below the soil surface are shown in Table 3. This design combines Tables 1 and 2 in a balanced two-way factorial experiment that allows yield response to surface or subsurface placement of nutritionally equivalent organic and inorganic amendments to be attributed to: a carbon, microbial or ‘organic matter’ effect, a nutrition effect, the amelioration of physicochemical constraints, or some factor relating to the depth of placement.

injected into discrete bands. Depending on the width of experimental plots, tillage machinery and sowing equipment, crop rows may be sown directly on top of amended bands (Fig. 3a) or alternately sown over amended or un-amended soil (Fig. 3b) (as per Celestina et al., 2018; Gill et al., 2012). The crop sampling protocol must be appropriate to capture this spatial heterogeneity, with a representative area comprising an equal ratio of amended to un-amended crop rows collected for analysis. Where all crop rows are sown on top of amended soil (Fig. 3a), normal plot sampling procedures can be followed as all rows are subject to the same treatment. However, where crop rows are alternately sown on top of amended and un-amended soil (Fig. 3b), the correct sampling protocol to capture this spatial heterogeneity would be to harvest the repeated unit. For example, if the amendment bands were in discrete rip lines spaced 0.8 m apart this would mean harvesting crop rows across the width of the plot in multiples of 0.8 m, since the repeated unit of amendment placement is 0.8 m wide sections of the plot (Fig. 3c). This procedure ensures that the correct ratio of crop rows sown over amended and un-amended soil is preserved. Depending on the region and farming system where the experiment is conducted (e.g. high rainfall raised beds vs low rainfall broadacre) it may be necessary to consider larger plots, the exclusion of border rows or the inclusion of rows beyond the rip line for the accurate estimation of yield (Rebetzke et al., 2014). The optimal area of harvested crop will depend on a range of factors that will vary from experiment to experiment (e.g. harvest equipment, soil heterogeneity) but must be large enough to maximize treatment differences whilst minimizing the effects of confounding variables (Rebetzke et al., 2014). 3.4. Additional measurements to separate factors contributing to yield responses Because organic amendments can have complex and interrelated plant nutrition and soil physicochemical amelioration effects, accurate measurements need to be made of a range of variables to identify which factors may be driving crop yield responses and to what extent. Exactly which measurements are taken will depend on the research question being posed and may include assessments of soil properties, nutrient balance, yield components and plant water use. If the amendments contain significant amounts of plant nutrients then the nutrient balance should be assessed by analyzing the macro- and micronutrient content of the amendment, the soil pre- and post-treatment, and the plant tissues at critical growth stages. If the organic amendment is also expected to contribute to crop yield increases via other mechanisms (e.g. improved soil structure, microbial activity) then changes in soil physical, chemical and biological properties before and after treatment also need to be assessed to determine if the organic amendment has affected plant yields via its effect on these properties. Analysis of root and shoot biomass at key growth stages and yield components at maturity (plant density, numbers of tillers and heads per plant or per unit area, grains per head or per unit area, grain size) can also aid interpretation of the source and regulation of the yield response (Slafer et al., 2014). Careful measurement using appropriate experimental controls will assist elucidation of the mechanisms responsible for yield responses. Quantification of the impact of these individual measures on crop yield may require the use of controlled environment experiments and simulation modelling in addition to field experimentation.

3.3. Appropriate sampling protocols to assess grain yield responses Spatially variable distributions of nutrients can occur where amendments are not evenly broadcast or incorporated into the soil profile. Subsoil incorporation of amendments, for example, creates spatially variable distributions of nutrients compared to an evenly applied surface control because the amendment is often incorporated or Table 2 Minimum tillage and amendment treatments required to separate effects on yield due to nutrition or other factors in experiments where organic matter is placed below the soil surface.

3.5. Long-term experimentation Responses to organic amendments and fertilizers can be seasonally dependent so it is important to conduct experiments over a number of sites and years to account for variability in seasonal conditions, soil types, yield potential and farming practices. Additionally, organic amendments may have cumulative effects or take time for effects to be measured and so need to be tested over longer time periods (Abbott et al., 2018; Diacono and Montemurro, 2010; Edmeades, 2003). 140

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Fig. 2. Possible outcomes from subsoil manuring experiments comprising a factorial combination of ± organic amendment and ± deep tillage.

Wherever possible – given monetary, personnel and other constraints on the research program – we recommend including long-term experiments (Johnston and Poulton, 2018) to contrast effects over shortterm (< 1–2 years), intermediate and long-term (> 5–10 years) timescales. In addition, for results to be more generally valid, it would be beneficial for experiments to be carried out on a wide range of sites with varied soil and climatic characteristics (Oelofse et al., 2015).

3.6. Controlled environment experiments Laboratory experiments conducted under controlled conditions can be used to overcome some of the limitations of field experiments, as well as increase our mechanistic understanding of the processes underlying the crop yield response. In field experiments it is often difficult to quantify the impact of a measured variable (e.g. soil N or 141

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Table 3 Complete tillage and amendment treatments required to separate effects on yield due to nutrition or other factors in experiments where organic and inorganic amendments are placed below the soil surface.

Fig. 3. Top and side view of experimental plots demonstrating the spatial heterogeneity that can arise from subsoil placement of amendments (a, b) and the appropriate sampling strategy to assess yield when crop rows are alternately sown over amended and un-amended soil (c).

aggregation) on crop yield because that environment is inherently complex and characterized by interactions between the plant, the soil and the amendment applied. Laboratory incubations and soil column experiments can assess the impact of these individual variables on the plant by controlling for other sources of variation in the experimental system. For example, although the nutrient effect may drive crop yield responses in the long term, the ‘organic matter effect’ may impact the plant in the short term via localized effects on bulk density and water availability that promote germination and early vigor (Mandal et al., 2013; Nyakatawa and Reddy, 2000b; Önemli, 2004). These mechanisms that operate over different temporal and spatial scales may not be apparent in larger-scale field experiments. Critically, controlled environment experiments can address confounding variables such as seasonal variation, soil profile heterogeneity or differing nutrient release rates.

a wide range of locations, climactic conditions and time periods. Additionally, modelling could be used to sensitively quantify the impact of individual variables on crop yields after the addition of amendments. There are a wide range of simulation models available (Salo et al., 2016) and so the choice of model will largely depend on the research question being asked. Crop yield responses to organic and inorganic fertilizer management practices in China have been tested using the Environmental Policy Integrated Climate (EPIC) model (Zhang et al., 2018), whilst the Crop Environment REsource Synthesis (CERES) model has been used to simulate crop and soil responses to compost application in France (Gabrielle et al., 2005). The Agricultural Production Systems sIMulator (APSIM) (Keating et al., 2003) has been used to simulate the impact of subsoil constraints on crop yields in Australia (Hochman et al., 2007; Rodriguez et al., 2006) and the yield and economic benefits of subsoil amelioration (Farre et al., 2010; Wong and Asseng, 2007). Both field and laboratory experiments can be used to calibrate and validate these models.

3.7. Modelling Simulation modelling may also be used to complement field and controlled environment experiments. Such modelling approaches allow for crop yield responses to organic amendments to be extrapolated over

4. Conclusion Experiments on the use of organic amendments as alternatives to 142

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inorganic fertilizers or soil ameliorants require the inclusion of necessary treatments to distinguish if yield responses are due to nutrients contained in amendments alleviating a nutritional constraint, or to improvement in soil physical or chemical properties. Experiments that do have appropriate treatments indicate that organic amendments and inorganic fertilizer, under the conditions of these experiments, can be equally effective at increasing crop yields on degraded soil when their nutrient content is balanced. Taken together, results indicate that nutrients may play a larger role in the crop yield response to organic amendments than physicochemical soil restoration or amelioration. In order to attribute the crop yield response to organic amendment to nutrition, soil physical or chemical improvement or some other factor, field experiments on the use of organic amendments must:

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i Identify a genuine and measurable constraint to crop yields at the experimental site; ii Incorporate proper controls, including matched mineral nutrients and surface applications of amendments in experiments investigating subsoil placement; iii Assess treatment differences using appropriate sampling protocols for crop growth and yield that adequately allow for spatial variation of application methods; iv Carry out appropriate soil and plant analyses to elucidate mechanisms responsible for yield responses; and v Be conducted over a number of sites and years to account for variability in seasonal conditions, soil types and farming practices. In addition, controlled environment experiments and simulation modelling may be used to complement experiments carried out in the field. These approaches can overcome some of the limitations of field experiments, as well as provide a detailed mechanistic understanding of the processes underlying crop yield responses. This review has strictly focused on the attribution of crop yield responses to organic amendments, and the design, conduct and evaluation of such experiments. It has not been our intention to evaluate the impact of organic amendments on other aspects such as soil health, long-term sustainability or ecosystem services. Additionally, it is not in contention that organic amendments, and organic matter in soils, have myriad benefits beyond their impact on soil fertility and plant nutrition. Instead, this review has demonstrated that there are multiple factors that can contribute to crop yield responses to organic amendments, and that attribution of yield responses to one factor or another is difficult without properly designed and monitored experiments outlined above. Conflict of interest The authors have no conflict of interest to declare. Acknowledgements This work was supported by a Grains Research and Development Corporation (GRDC) Grains Industry Research Scholarship (GRS11004). References Abbott, L.K., Macdonald, L.M., Wong, M.T.F., Webb, M.J., Jenkins, S.N., Farrell, M., 2018. Potential roles of biological amendments for profitable grain production—a review. Agric. Ecosyst. Environ. 256, 34–50. https://doi.org/10.1016/j.agee.2017. 12.021. Adcock, D., McNeill, A.M., McDonald, G.K., Armstrong, R.D., 2007. Subsoil constraints to crop production on neutral and alkaline soils in south-eastern Australia: a review of current knowledge and management strategies. Aust. J. Exp. Agric. 47, 1245–1261. https://doi.org/10.1071/EA06250. Adeli, A., Dabney, S.M., Tewolde, H., Jenkins, J.N., 2017. Effects of tillage and broiler litter on crop productions in an eroded soil. Soil Tillage Res. 165, 198–209. https:// doi.org/10.1016/j.still.2016.08.010. Agbede, T.M., Ojeniyi, S.O., 2009. Tillage and poultry manure effects on soil fertility and

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