The synchrony of cover crop decomposition, enzyme activity, and nitrogen availability in a corn agroecosystem in the Midwest United States

Soil & Tillage Research 197 (2020) 104518

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The synchrony of cover crop decomposition, enzyme activity, and nitrogen availability in a corn agroecosystem in the Midwest United States

T

Clayton J. Nevins, Corey Lacey, Shalamar Armstrong* Department of Agronomy, College of Agriculture, 915 West State Street, Purdue University, West Lafayette, IN 47907, United States

A R T I C LE I N FO

A B S T R A C T

Keywords: Nitrogen availability Soil enzyme activity Cover crops No-tillage Soil microbial community Nitrogen cycling Carbon cycling

Cover cropping is commonly associated with increased soil microbial activity and soil health. Cover cropping in the Upper Mississippi River Basin has increased rapidly in the last decade due to the demonstrated ability that cover crops can increase soil health and decrease nitrate losses in tile-drained fields. One reason cover cropping is not adopted in the Midwest United States is the lack of knowledge on the synchrony of cover crop residue nitrogen (N) release and corn N demand. Therefore, the overarching goal of this research was to investigate soil enzyme activity and inorganic N availability during the decomposition period of common winter cover crops. Objectives were: i) to determine if soil enzyme activity (β-glucosidase and urease) is influenced by different cover crops (cereal rye (CR), hairy vetch (HV), and HV/CR mixture) and tillage systems (reduced tillage and notillage residue management) during the residue decomposition period, and ii) to determine the relationship between soil enzyme activity, inorganic N availability, and critical corn growth stages during cover crop decomposition. Cover crops in this study were selected due to contrast in residue carbon (C):N ratios, their commonality among regional farmers, and their differences in physiology. Spring tillage and no-tillage were investigated because of the differing levels of soil disturbance and residue incorporation. Enzyme activities were quantified at seven sampling dates following cover crop termination from April-October during the 2016 and 2017 corn growing seasons. Results revealed significant effects of sampling date (p < 0.001) and cover crop treatment (p < 0.05) on soil β-glucosidase activity and significant interaction effects between sampling date and cover crop treatment (p < 0.05) on potential soil urease activity. Tillage had a significant impact on soil βglucosidase (p < 0.001) and urease (p < 0.05) activities in 2017, with higher activity observed in the notillage soil. These findings indicate that enzyme activity fluxes can be observed in agroecosystems one year after introducing conservation practices, such as cover crops and no-tillage. Greater than 50 % of C release from cover crop residue occurred from corn emergence to tasseling, and significantly greater β-glucosidase activity for CRbased treatments during corn peak N demand did not result in more soil inorganic N. This indicates a loss of plant-available N from the agroecosystem, which could be attributed to N immobilization by the soil microbial community. This study demonstrates a need to develop adaptive N fertilization management for corn that can overcome the potential impact of N immobilization during peak corn N demand following CR.

1. Introduction Cover crops and reduced tillage systems are being incorporated into conventional cropping systems to reduce water and wind soil erosion (Dabney, 1998; Decker et al., 1994; Delgado et al., 1998; Langdale et al., 1991), increase soil health (Liu et al., 2005), and to scavenge nitrogen (N) from the soil profile to improve water quality (Kaspar and Singer, 2011; Lacey and Armstrong, 2014; Roth et al., 2017; Ruffatti et al., 2019). Cover crops have been reported to have positive (Coombs et al., 2017; Marcillo and Miguez, 2017), neutral (Finney et al., 2016; Gieske et al., 2016; Noland et al., 2018) and negative (Kaspar and ⁎

Bakker, 2015) effects on corn yield, with negative effects potentially caused by cereal rye (Secale cereale) (CR) allelopathic effects on corn (Weston, 1996). Nitrogen scavenged during the growth of cover crops, such as CR, is assimilated into the cover crop biomass leading to carbon (C):N ratios ranging from 10-38:1, in some cases (Fageria et al., 2005; Sainju and Singh, 1997; Singh et al., 2018; Villamil et al., 2006; Weinert et al., 2002). Thus, there is an influx of labile C from the cover crop biomass into the soil system during decomposition after cover crop termination. It has been documented that this influx of labile C has resulted in a decrease in the availability of soil N due to immobilization, especially when following CR cover crops, leading to reduced corn yield

Corresponding author. E-mail address: [email protected] (S. Armstrong).

https://doi.org/10.1016/j.still.2019.104518 Received 20 December 2018; Received in revised form 21 November 2019; Accepted 22 November 2019 0167-1987/ © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).

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activity linked to the C and N cycles and soil N availability during corn development following cover crop termination. The overarching goal of this research was to investigate the dynamics of potential soil enzyme activity and inorganic N availability during the decomposition period of winter cover crops in reduced spring tillage and no-tillage residue management systems. Specifically, the objectives were: i) to determine if potential enzyme activities (β-glucosidase and urease) are influenced by different cover crops and tillage systems during the residue decomposition period, and ii) to determine the relationship between enzyme activity, soil inorganic N availability, and critical corn growth stages during the cover crop decomposition period. Understanding the dynamics of potential enzyme activity, and subsequently, inorganic N availability, during the cover crop decomposition period could enhance our understanding of the synchrony between cover crop N release and corn N demand.

(Crandall et al., 2005; Kessavalou and Walters, 1999; Krueger et al., 2011; Roth et al., 2017; Tollenaar et al., 1993). Nitrogen immobilization in the case of CR is driven by increased demand on soil available N that is attributed to the generation of new microbial biomass as a product of C release and the metabolizing of N poor residue, such as CR. Nitrogen immobilization results in a lack of corn (Zea mays) N uptake and reduced yields relative to the no cover crop control. Thus, one of the barriers to widespread cover crop adoption is the lack of understanding of how cover crop residue will impact available N during the peak N demand of the corn cash crop (Snapp et al., 2005; Snapp and Borden, 2005; Snapp and Fortuna, 2003). Developing a better understanding of the availability of N during cover crop decomposition and the cash crop growing season could lead to increased adoption of cover crops among farmers who currently hesitate to incorporate these practices in agroecosystems because of the potential for N immobilization at cash crop critical N-demanding growth stages. Furthermore, increasing the adoption of cover crops in the U.S. Corn Belt has the potential to increase soil health and decrease nitrate loading to the Mississippi River (Dabney, 1998). Additionally, legume cover crops, such as hairy vetch (HV) (Vicia villosa), which mineralize N faster relative to rye (Rosecrance et al., 2000), have been shown to increase inorganic N following termination during the peak N demand of the cash crop (Kuo et al., 1997), which could contribute to cash crop yield. This increased availability of inorganic N relative to rye could be attributed to a decreased C:N ratio of HV residue. While studies have investigated the impact of cover cropping and reduced tillage on changes in soil microbial community composition (Degrune et al., 2017; Fernandez et al., 2016; Nevins et al., 2018), phospholipid fatty acid profiles (Finney et al., 2017), and soil biochemical properties (Acosta-Martinez et al., 2011; Simmons and Coleman, 2008), there is still a lack of consensus surrounding the effects of these management practices on the dynamics of potential soil enzyme activity, soil N availability, and the relationship between these during cover crop decomposition and at critical N demanding corn growth stages. A link between C and N cycling enzyme activity and inorganic N has been confirmed in the context of agroecosystem management practices (Bowles et al., 2014), but this link is usually investigated with relation to a single sampling date. Likewise, it is common for cover crop studies to examine the impacts of organic amendments by soil sampling prior to cover crop termination or planting (Bandick and Dick, 1999; Fernandez et al., 2016). However, there is evidence that potential enzyme activities and inorganic N availability have high in-season variability (Bell et al., 2009a,b; Debosz et al., 1999), and this in-season variability could be impacted by the addition of organic amendments, which are an energy source for the microbial community as C and N are released. Potential enzyme activity assessments have been used as complements to other soil nutrient analyses because enzyme activity is the driver of organic matter decomposition through chemical reactions (Allison et al., 2007). Additionally, potential enzyme activities have been used to understand microbial functional response to soil conditions because soil extracellular enzyme activity represents the microbial metabolic requirements (Bell et al., 2009a,b; Caldwell, 2005). Specifically, the enzyme β-glucosidase depolymerizes cellulose, the most common polysaccharide in nature, yielding glucose (Acosta-Martínez et al., 2019). The enzyme urease hydrolyzes pools of organic N (Tabatabai and Bremner, 1972). The enzyme activity of β-glucosidase and urease are indicators for the potential degradation of C polymers and the release of ammonia, respectively (Dilly et al., 2003). Both βglucosidase and urease activity have been found to be highly responsive to nutritional conditions (Dilly et al., 2007; Dilly and Nannipieri, 2001), but this response has not been observed during the decomposition period of winter cover crops at corn critical growth stages. To advance our understanding of in-season dynamics and timing of N availability in cover cropped agroecosystems, we used a time series sampling technique to quantify the in-season dynamics of soil enzyme

2. Materials and methods 2.1. Research site and field activities The research site was located at the Purdue University Agriculture Center for Research and Education in Tippecanoe County Indiana on a silty clay loam soil (fine-silty, mixed, mesic Typic Haplaquolls). Prior to beginning the project, soil fertility was corrected to be even across the plots. At the start of the project, soil phosphorus and potassium concentrations were on average 25 mg kg−1 and 111 mg kg−1, respectively. Soil pH was on average 6.5. Soil C and organic matter were 2.1 % and 3.8 %, respectively. The winter of 2015/2016 was the first year the cover crop and tillage treatments were implemented. Prior to these cover crop and tillage regimes the site was a corn-soybean annual rotation with spring tillage prior to corn planting. The experiment had a split-plot design with three field replications. Two experimental factors, cover crop and tillage, were used to form six treatments. Treatments included HV, CR, and a HV/CR mixture (mixture) and each received two levels of residue management, including reduced tillage and no-tillage. Each plot was 12 rows wide and approximately 80 m in length with 76 cm (30-inch) corn rows. Cover crops were planted on September 28–30, 2015 and September 19, 2016 during the first and second years of the study, respectively. In September 2015, cover crops were drilled after harvest and the HV and CR seeding rates were 34 and 56 kg ha−1 drilled, respectively. The HV/ CR mixture was drilled at a rate of 17/45 kg ha−1. In September 2016, cover crops were inter-seeded before soybean leaf drop and the HV and CR seeding rates were 67 and 112 kg ha−1, respectively. The HV/CR mixture seeding rate was 28/84 kg ha−1. Cover crops grew over the winter and spring and were chemically terminated on April 14 in both years of the study. Following termination each year, anhydrous ammonia was applied as an injection at a rate of 200 kg N ha−1 on April 19, 2016 and April 22, 2017. Fertilization using anhydrous ammonia is a common practice among farmers in this region (Eckert, 1991; Bavin et al., 2009). The reduced tillage residue management plots received disk tillage in the spring that incorporated the terminated cover crop residue to a depth of 15 cm. In the first year of the study, spring tillage plots were disk tilled twice to a depth of approximately 15 cm on April 25, 2016. The plots were cultivated to prepare the seedbed and corn was planted on April 26, 2016. In the second year of the study, the spring tillage plots were disk tilled twice on May 18, 2017. The plots were cultivated and corn was planted on May 30, 2017. The no-tillage plots were not disked in the spring. The overall corn yield among treatments was 14.1 ± 0.9 Mg ha−1 and 12.1 ± 1.9 Mg ha−1 in 2016 and 2017, respectively. 2.2. Cover crop biomass collection to determine winter and spring growth Cover crop aboveground biomass was collected before cover crop 2

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litter bags with 1 mm mesh openings. The mixture treatment litter bags were created using litter harvested from CR and HV plots to ensure the same amount of CR and HV were added to each mixture bag. Litter bags for the mixture treatment consisted of 20 % HV and 80 % CR to approximate the biomass composition in the mixture plots. Both the reduced spring tillage and no-tillage treatments received CR, HV, and mixture litter bags. Litter bags were place on May 1, 2016 and May 9, 2017. No-tillage litter bags were placed on the soil surface using garden staples to prevent loss or movement of litter bags. The reduced spring tillage treatments were simulated by burying litter bags to a depth of 7.5 cm (half the tillage depth). In both years, litter bags were collected near enzyme soil sampling dates to closely approximate enzyme activity and litter bag C release. At collection, one litter bag was sampled from each plot. Litter bags were gently rinsed, oven dried, and ground. Ground litter was then analyzed for C and ash content. Carbon content was determined using dry combustion analysis (Flash 2000 Elemental Analyzer, CE Elantech, Lakewood, NJ). Litter bag residue weight was calculated on an ash free basis by ashing 1 g subsample at 500 °C for 4 h. Cumulative litter bag C release for each sampling date was calculated by multiply the percent C and the ash-free dry mass weight for that date (Nelson and Sommers, 1996; Ruffo and Bollero, 2003; Sievers and Cook, 2018), allowing for an estimate of C release for each cover crop treatment (species x tillage) and sampling date.

Table 1 Corresponding soil sampling dates, days after cover crop termination, and corn growth stages during the 2016 and 2017 corn growing seasons. Soil Sampling Date

Days after Cover Crop Termination

Corn Growth Stage

4/20/2016 4/26/2016 5/5/2016 5/23/2016 6/6/2016 6/28/2016 8/1/2016 9/23/2016

6 12 21 39 53 75 109 162

Pre-plant Corn planted VE V3 V6 VT R2 R6

4/20/2017 5/8/2017 5/30/2017 6/28/2017 7/31/2017 8/21/2017 10/8/2017

6 24 46 75 108 129 177

Pre-plant Pre-plant Corn planted V6 VT R2 R6

2016

2017

termination in April of 2016 and 2017 to determine the amount of winter and spring biomass accumulation. Biomass was collected using 1 m2 quadrants placed randomly in each plot. Biomass was oven dried at 60 °C, ground, and C and N content were determined using dry combustion analysis (Flash 2000 Elemental Analyzer, CE Elantech, Lakewood, NJ).

2.6. Soil β-glucosidase activity

Soil samples were collected at seven dates during both the 2016 and 2017 corn-growing seasons, with each soil sampling date corresponding to a specific number of days after cover crop termination and the approximate growth stage of the corn cash crop at the sampling date (Table 1). During each sampling, 15 randomly distributed soil cores (not intact) were removed per plot at a depth of 4 cm using a 4 cm diameter soil probe. The cores were homogenized during sampling to create a composite bulk sample for each plot. The bulk samples were transported from the field to the lab on ice in a cooler. Approximately 100 g of each bulk sample was stored at 4 °C for enzyme assays. An additional subsample of the bulk soil was air-dried and used for physicochemical analyses.

Potential soil β-glucosidase activity (μmoles para-nitrophenol released g dry soil−1 hr−1) was quantified according to Eivazi and Tabatabai (1988). Enzyme assays were completed within 48 h of soil sampling and stored at 4 °C until analysis. Briefly, soil was sieved (< 2 mm) and ∼1 g was weighed into Erlenmeyer flasks. Triplicates were performed for each soil sample, as well as a negative control and substrate control. Each of the Erlenmeyer flasks were treated with 0.2 mL of toluene, the solution was mixed, and remained in the fume hood for 15 min. Flasks were then treated with 4 mL of a modified universal buffer (MUB) (pH 6.0) and 1 mL of para-nitrophenyl-β-Dglucoside (PNG) (50 mM). Substrate control flasks were not treated with PNG. The flasks were stoppered, mixed thoroughly, and incubated at 37 °C for 1 h. After incubation, 1 mL of CaCl2 (0.5 M) and 4 mL of tris (hydroxymethyl)aminomethane (THAM) buffer (100 mM, pH 12) were added and the product was filtered. The yellow intensity of the color reaction was measured on a spectrophotometer at 415 nm.

2.4. Soil physicochemical analysis and weather data collection

2.7. Soil urease activity

Soil moisture was determined by oven drying a subsample of the fresh, 2 mm sieved soil at 105 °C for 48 h. Nitrate (NO3−-N) and ammonium (NH4+-N) (combined to form total inorganic N) were measured on the air-dried soil by shaking 2 g with 20 mL of 1 M KCl for 1 h on a rotary shaker. The soil extracts were centrifuged for 2 min and filtered. The supernatants were analyzed on a SEAL AQ2 analyzer (Mequon, Wisconsin) using USEPA methods 353.2 ver.2 and 350.1 ver.2 (USEPA, 1993). Precipitation and bare soil temperature measurements specific to the research site were collected from the Indiana State Climate Office (https://iclimate.org).

Potential soil urease activity (μg NH4-N g dry soil−1 2 hr−1) was quantified according to Kandeler and Gerber (1988). Triplicates were performed for each sample, as well as a negative and substrate controls. Briefly, the flasks were treated with 2.5 mL of urea (720 mM) substrate solution and 20 mL of borate buffer (0.1 M, pH 10). The flasks were stoppered and incubated at 37 °C for 2 h. After incubation, flasks were treated with 30 mL of potassium chloride (2 M)-hydrochloric acid (0.01 M) solution. Samples were placed on a rotary shaker for 30 min at 100 rpm, and soil suspensions were filtered following shaking. The NH4+-N released during incubation was determined by combining a 1 mL subsample of the filtrate and 9 mL of Nanopure (Thermo Scientific, Barnstead Nanopure) water. A standard curve was prepared by mixing 1 mL of ammonium chloride standards containing 0, 2.5, 5, 10, 15, 20, 25, and 30 μg NH4-N mL−1 with 9 mL of Nanopure (Thermo Scientific, Barnstead Nanopure) water. For the color reaction to take place, 5 mL of sodium salicylate (1.06 M)-sodium hydroxide (0.3 M) solution and 2 mL of sodium dichloroisocyanurate (3.91 mM) solution were added to the extracts and the standards. The tubes were swirled for a few seconds for adequate mixing and the color developed for 30 min at room temperature. The absorbance of the extracts and

2.3. Soil sampling

2.5. Cover crop carbon release To estimate C release from cover crop treatments, a supporting litter bag study was conducted during the same time period and for the same treatments (CR, HV, and mixture) as the main study. Cover crop shoot biomass was harvested from respective CR and HV plots. A subsample of this material was collected, dried, ground and analyzed for initial N content. Twenty grams of air-dried, not ground, cover crop residue material was then weighed and placed into 30 × 15 cm nylon mesh 3

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standards were measured at 660 nm on a spectrophotometer.

Table 2 Summary of average cover crop biomass (kg biomass ha−1) and C:N ratios after winter growth before termination. Letters indicate significant differences in biomass and C:N ratio between treatments within year. Data are formatted as mean ± std and statistical significance is p < 0.05.

2.8. Statistical analyses A two-way analysis of variance (ANOVA) was used to determine the statistical significance of the treatment main effects using the MIXED procedure in SAS v. 9.3 (SAS Institute, 2007) for the cover crop C release. Differences in means were determined using a Tukey adjustment, and an alpha level of 0.05 was used to determine significant differences. Enzyme assays were completed in laboratory triplicates, and the mean of the triplicates was used for statistical analysis. A single inorganic N (NO3-−N and NH4+-N) value was collected for each soil sample and was used for statistical analysis. Analysis of variance of potential soil β-glucosidase and urease activities and inorganic N was analyzed using linear mixed models (SAS Institute, 2007). Sampling date, cover crop (main plot) and tillage (subplot) were each considered fixed effects and block was a random effect. Sampling date was modeled as a repeated measure and the Tukey-Kramer adjustment was used to consider all pairwise comparisons.

2016 Biomass (kg ha Cereal Rye Mixture Hairy Vetch

1858 ± 407a 1967 ± 795a 418 ± 259b

2017 −1

)

C:N ratio 16.6 ± 0.7a 16.0 ± 0.8a 12.9 ± 1.1b

Biomass (kg ha−1) 888 ± 234a 916 ± 325a 512 ± 403a

C:N ratio 21.1 ± 0.35a 20.5 ± 1.20a 11.9 ± 0.85b

3.2. Cover crop winter and spring biomass accumulation In 2016, average cover crop aboveground biomass was 1967 and 1858 kg ha−1 in the mixture and CR plots, respectively, which was significantly more biomass relative to HV plots (418 kg ha−1) (p < 0.05). In 2017, the CR (915 kg ha−1) and mixture (888 kg ha−1) treatments had more aboveground biomass relative to the HV (512 kg ha−1) treatment, but this trend was not significant (p > 0.05). Therefore, there was more than double the amount of aboveground biomass available for decomposition in 2016 compared to 2017 in the mixture and CR treatments, respectively, but in the HV treatment, there was an additional 96 kg biomass ha−1 available for decomposition in 2017 compared to 2016. In 2016, the average C:N ratios of the CR, mixture and HV treatments were 16.6, 16.0, and 12.9, respectively. In 2017, the average C:N ratios of the CR, mixture and HV treatments were 21.1, 20.5, and 11.9, respectively (Table 2).

3. Results 3.1. Weather conditions The spring (April-May) of 2016 and 2017 were warmer than the 30 yr air temperature averages, and the spring of 2017 was an average of 1.9 °C warmer than the spring of 2016. Soil temperatures peaked in 2016 later in the corn growing season (mid-August at > 31.5 °C) compared to 2017 temperatures, which peaked on July 7 (Fig. 1A-B). There was 26 % more total precipitation during the 2017 corn growing season (749 mm) compared to the 2016 period (548 mm). April received over a third more precipitation in 2017 (109 mm) compared to 2016 (67 mm). This precipitation delayed corn planting until May 30 in 2017, which was later than 2016 and the average historical planting date among farmers in West Central Indiana.

3.3. Cover crop carbon release during decomposition Significant effects of both cover crop (p < 0.05) and tillage (p < 0.05) on C release from cover crop biomass were observed in both 2016 and 2017 (Fig. 2). In 2016, for both CR and the mixture, the reduced tillage treatments resulted in significantly greater C release

Fig. 1. Weather parameters (daily precipitation and bare soil temperature) during the (A) 2016 and (B) 2017 cover crop decomposition periods. 4

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Fig. 2. Cover crop carbon release in (A) 2016 and (B) 2017. Error bars represent one standard error from the mean.

glucosidase activity significantly increasing at 39 days after termination for all cover crop treatments. For all treatments except HV, there was significantly greater activity at the V6 growth stage relative to V3 (p < 0.05). At 53 days after termination (V6), during peak activity among all treatments, CR and mixture treatments had significantly higher activity compared to the HV (3.69 μmoles para-nitrophenol released g dry soil−1 hr−1) and control (4.18 μmoles para-nitrophenol released g dry soil−1 hr−1). Potential soil β-glucosidase activity in all treatments remained at a somewhat constant level from 75 days after termination through 162 days after termination but was significantly greater than that observed from 6 to 21 days after termination (p < 0.05). In 2017, though not as pronounced as 2016, potential soil β-glucosidase activity significantly increased in all cover crop treatments when averaged across tillage treatments during the corn growing season (p < 0.05) (Fig. 3B). Different from 2016, the potential soil βglucosidase activity in 2017 was less dynamic. Activity for all cover crop treatments significantly increased from 6 to 24 days after cover crop termination (p < 0.05). Due to a late corn planting, these sampling dates were prior to corn emergence. This was unlike 2016, when the significant increase in soil β-glucosidase activity occurred after corn planting. From 24 to 75 days after termination, the potential activity of all treatments remained relatively constant and then significantly decreased from 108 to 129 days after termination. Similar to during peak activity from 24 to 75 days after termination, potential activity was significantly higher in the CR and mixture treatments than the HV treatment (p < 0.05) and trended greater than the control from 108 to 129 days after termination. In 2017, the no-tillage treatments averaged higher activity (2.48 μmoles para-nitrophenol released g dry soil−1 hr−1) than the spring tillage treatments (2.34 μM para-nitrophenol released g dry soil−1 hr−1) when averaging across cover crop treatments.

when compared to the no-tillage treatments. The greatest impact of tillage occurred 39 days after termination. At 39 days after termination the CR and mixture reduced tillage treatments were 199 kg ha−1 and 238 kg ha−1 significantly greater than CR and mixture no-tillage treatments, respectively (Fig. 2). In contrast, tillage did not significantly impact the HV C release in 2016 (p > 0.05). However, across the reduced tillage and no-tillage treatments, the HV treatment always resulted in significantly less C release than the treatments with CR (p < 0.05). For all treatments, greater than 50 % of potential C release occurred 39–75 days after termination (between V3 and VT). Furthermore, for HV only treatments, 50 % of C release occurred by 21 days after termination (after emergence). By 178 days after termination (harvest) nearly all potential C input (> 95 %) had occurred for all treatments. There were significantly less C inputs for CR and mixture treatments in 2017 relative to 2016 (p < 0.05). This is the result of less CR winter growth in the second year of the study. Similar to 2016, HV C input was significantly less than the CR and mixture treatments. Unlike in 2016, reduced tillage resulted in significantly greater C releases for all cover crop treatments, including HV, at all sampling dates except at 184 days after termination. The largest effect of tillage was observed 61 days after termination when HV, CR, and mixture reduced tillage treatments resulted in 65.6, 155.1, and 157.5 kg ha−1 greater cumulative C release relative to their respective no-tillage treatments. All treatments reached greater than 50 % total C release between 46–108 days after termination. Similar to 2016, nearly all (> 95 %) of C release had occurred for all treatments by harvest. 3.4. Cover crops, tillage, and sampling date influenced soil enzyme activities during the cover crop decomposition period 3.4.1. Potential soil β-glucosidase activity Significant effects of both sampling date (p < 0.001) and cover crop treatment (p < 0.05) on potential soil β-glucosidase activity were observed in 2016 and 2017. Tillage resulted in a significant decrease in activity in 2017 (p < 0.05) but not in 2016 (Table 3). There were no significant interactions between sampling date, cover crop treatment, or tillage treatment in either season (Table 3; Fig. 3A). In 2016, potential soil β-glucosidase activity for all treatments was characterized by a linear increase in activity from cover crop termination to the V6 corn growth stage (53 days after termination) and a linear decline from V6 to harvest. The β-glucosidase activity for all treatments was statistically similar from 6 to 21 days after termination, but activity at this time was significantly lower relative the activity at 39 (V3) and 53 (V6) days after termination (p < 0.05). Corn planting occurred 12 days after cover crop termination in 2016, which was prior to soil β-

3.4.2. Potential soil urease activity There were significant interaction effects between sampling date and cover crop treatment on potential soil urease activity during the 2016 and 2017 cover crop decomposition periods (p < 0.05) (Table 3). Tillage treatment had a significant effect on potential urease activity in 2017 (p < 0.05), but not 2016 (p > 0.05). In 2016, potential soil urease activity increased with soil temperature in all cover crop treatments when averaged across tillage treatments until the final sampling date when the corn was at physiological maturity 162 days after cover crop termination (Fig. 4A). Thus, for all treatments, urease activity was significantly greater relative to the activity at cover crop termination (p < 0.05). Potential activity significantly increased for all treatments from near cover crop termination (6 days after termination) to 21 days after termination (p < 0.05). At 21 days after termination, the control 5

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Table 3 Analysis of variance summary table for response variables soil β-glucosidase activity, urease activity, and inorganic nitrogen. β-glucosidase

Date Cover Crop Tillage Date*Cover Crop Cover Crop*Tillage Date*Tillage Cover Crop*Tillage*Date

Urease 2016 < 0.001 0.025 NS NS NS NS NS

2017 < 0.001 0.002 < 0.001 NS NS NS NS

2016 < 0.001 0.009 NS 0.033 NS NS NS

treatment (44 μg NH4-N g dry soil−1 2 hr−1) had significantly lower activity than the CR (59 μg NH4-N g dry soil−1 hr−1), mixture (58 μg NH4-N g dry soil−1 2 hr−1), and HV (56 μg NH4-N g dry soil−1 2 hr−1) treatments. Activity continued to increase in all treatments leading up to the highest activity at 53 and 75 days after termination, when the CR treatment (73 μg NH4-N g dry soil−1 2 hr−1) had significantly higher activity relative to the mixture (60 μg NH4-N g dry soil−1 hr−1), HV (47 μg NH4-N g dry soil−1 2 hr−1), and control (63 μg NH4-N g dry soil−1 2 hr−1) treatments (p < 0.05). The dynamics of potential soil urease activity in 2017 distinctly contrasted with the activity of 2016 as activity for all treatments decreased linearly with time. Specifically, in 2017, potential soil urease activity was not significantly different near termination (6 days after termination) compared to the sampling date when the corn was at maturity (177 days after termination) in the CR, HV, and control treatments when averaged across the main effect of tillage. At sampling dates from 6 to 75 days after termination, the HV activity was significantly lower than the CR, mixture, and control treatments. There was no significant difference in potential activity between cover crop treatments 108 and 129 days after termination, but at 177 days after termination the HV treatment (27 μg NH4-N g dry soil−1 2 hr−1) had significantly lower potential activity than the CR (36 μg NH4-N g dry soil−1 2 hr−1), mixture (40 μg NH4-N g dry soil−1 2 hr−1), and control (42 μg NH4-N g dry soil−1 2 hr−1) (p < 0.05). When averaging across cover crop treatments and sampling dates, the no-tillage (49 μg NH4-N g dry soil−1 2 hr−1) had significantly higher enzyme activity than the spring tillage (41 μg NH4-N g dry soil−1 2 hr−1).

Inorganic N 2017 < 0.001 0.008 0.031 0.021 NS NS NS

2016 < 0.001 NS < 0.001 NS NS < 0.001 NS

2017 < 0.001 NS NS NS NS 0.04 NS

greater in the spring tillage treatment compared to the no-tillage treatment from 39 to 109 days after termination when averaged across cover crop treatments at four consecutive sampling dates (p < 0.05) (Fig. 5A). By June 28 at VT (75 days after termination), the soil inorganic N available in the spring tillage plots peaked (90 mg kg−1 soil), and there was significantly more inorganic N available at this sampling date compared to any other sampling dates (p < 0.05). In 2016 and 2017, the average inorganic N during the decomposition period was 29 and 41 mg kg−1 soil, respectively. In 2017, soil inorganic N values in April and May from 6 to 46 days after termination were two-fold higher than in the same months in 2016. In 2017, soil inorganic N was significantly higher from 46 to 129 days after termination in the spring tillage treatments compared to the beginning and end of the corn growing season (p < 0.05). In the no-tillage treatment, inorganic N was significantly higher 75 days after termination compared to the other sampling dates (p < 0.05) (Fig. 5A). There was only one sampling date in 2017 when there was a significant difference in inorganic N between the spring tillage and no-tillage treatments (24 days after termination), and at this sampling date there was more inorganic N available in the no-tillage treatment (32 mg kg−1 soil) than the spring tillage (29 mg kg−1 soil) (p < 0.05). 4. Discussion Cover crops have the ability to scavenge or biologically fix N during the fallow period and release N during decomposition following termination (Jahanzad et al., 2016; Murungu et al., 2010). Understanding the dynamics of soil enzyme activity during cover crop residue decomposition gives insight on how the function of the soil microbial community responds to C release from cover crop residue, the synchrony of cover crop residue N release, and N demand of the growing cash crop (Jahanzad et al., 2016). In this study, we found that both cover crop species and tillage significantly impacted C release during cover crop residue decomposition. In both years of the study, HV residue decomposed at a faster rate relative to CR-based (CR and mixture)

3.5. Temporal fluctuations of inorganic nitrogen Cover crop treatment did not have a significant effect on inorganic N availability during the 2016 or 2017 seasons (p > 0.05) (Table 3). The interaction effect of sampling date and tillage on inorganic N availability was significant during both years of the study (Table 3) (p < 0.05). In 2016, soil inorganic N availability was significantly

Fig. 3. Average measured levels of potential soil β-glucosidase activity (μmoles para-nitrophenol released g dry soil−1 hr−1) in each cover crop treatment during the (A) 2016 and (B) 2017 corn growing seasons. Bars with the same letter are not significantly different from each other within cover crop treatment over the corn growing season as determined using PROC MIXED and a repeated measures model (p < 0.05). The whiskers indicate the lower (25 %) quartile and upper (75 %) quartile. 6

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Fig. 4. Average measured levels of potential soil urease activity (μg NH4-N g dry soil−1 2 h−1) in each cover crop treatment during the (A) 2016 and (B) 2017 corn growing seasons. Bars with the same letter are not significantly different from each other within cover crop treatment over the corn growing season as determined using PROC MIXED and a repeated measures model (p < 0.05). The whiskers indicate the lower (25 %) quartile and upper (75 %) quartile.

Fig. 5. Average soil inorganic nitrogen (mg inorganic N kg soil −1) for tillage and no-tillage residue management treatments during the (A) 2016 and (B) 2017 corn growing seasons. Bars with the same letter are not significantly different from each other within tillage treatment over the corn growing season as determined using PROC MIXED and a repeated measures model (p < 0.05). The whiskers indicate the lower (25 %) quartile and upper (75 %) quartile. Significant differences between tillage treatments within each sampling date are identified by an asterisk (*) directly above the day after termination on the x-axis (p < 0.05).

termination timing, fertilizer application, and corn planting can be weather dependent. This recommendation is to help farmers avoid N immobilization due to C release from CR residue. Our cover crop C release curves suggest that this recommendation in reference to C release and N immobilization is not entirely accurate, and that peak rates and mass of C release can occur later in the corn growing season between V6 and VT. Thus, it is likely that the process of N immobilization occurs outside of the two to three week window between cover crop termination and cash crop planting. This was also corroborated by the observed dynamics of soil β-glucosidase and urease enzyme activities during the cover crop residue decomposition periods. The dynamics of soil enzyme activity as cover crop residue decomposed were impacted by weather and soil temperature, which differed between 2016 and 2017. In 2016, the soil temperature increased and peaked in mid-August and 2016 received the least precipitation of the two years. During this increase, peak soil β-glucosidase activity occurred in early June at the V6 growth stage followed by the peak of both urease activity and soil inorganic N in late June at the VT corn growth stage. In contrast, possibly due to a warmer spring in 2017, the soil β-glucosidase and urease activity peaks occurred at planting in early May followed by the peak in inorganic soil N in late May to early June. It should be noted that anhydrous ammonia application occurred in mid-April in both years of the study. Application on April 19, 2016 was only seven days prior to corn planting in 2016, however, application on April 22, 2017 was 38 days prior to corn planting in 2017. Furthermore, we also discovered that the presence of CR residue in both years resulted in significantly greater soil β-glucosidase and urease activity, but did not translate into greater soil available N. These differences where more pronounced in 2016 when CR biomass was two

treatments. This could be attributed to a lower C:N ratio or the chemical composition of the residue, such as lignin concentration (Ruffo and Bollero, 2003). These findings aligned with the results of other researchers who found that enzyme activities varied based on cover crop treatment during the subsequent cash crop growth period (Bandick and Dick, 1999; Bowles et al., 2014; Fernandez et al., 2016). Reduced spring tillage that resulted in the incorporation of the cover crop residue significantly increased the decomposition rate of CR based treatments in both years of the study and in one of two years for HV. Tillage increases the rate of oxygen diffusion into the soil, which impacts microbial activity, and it reduces the size of the residue and increases soil to residue contact, all of which could contribute to greater rates of residue decomposition (Busari et al., 2015; Guérif et al., 2001; Zhang et al., 2018). In addition to the rate of decomposition of cover crop residue as affected by cover crop species and tillage, our data gives insight into the timing of C input into the soil from cover crop residue relative to corn growth and development. Despite cover crop species, biomass levels, and tillage, we observed the greatest mass of cover crop residue C release to the soil during the first 50–68 calendar days after cover crop termination. In terms of corn growth stages, this rapid influx of cover crop residue C occurred from corn emergence to V6-VT, depending on planting date. In fact, in both years of the study, greater than 50 % of C release had occurred by VT. According to conventional cover crop thought, this C input has been predicted to occur early in the growing season between cover crop termination and cash crop planting (Austin et al., 2017). Therefore, a common recommendation is to plant corn at least two to three weeks after cover crop termination, especially if the cover crop is CR or other species that commonly have high aboveground residue C:N ratios. Though, it is understood that cover crop 7

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growth. Identifying higher relative abundances of bacteria in the CR treatment that have previously been reported as being cellulolytic and have larger effects in differentiating the CR and HV treatments (Nevins et al., 2018) indicates that the soil microbiome may be more likely to utilize available N to continue metabolizing CR residue. This could lead to a lack of N present in solution to meet the demand of corn as the bacteria require N for metabolizing C. Thus, it is possible for N immobilization to occur during the peak N demand of the subsequent corn crop, which presents a need to develop N fertilization adaptive management practices that will help to mitigate N immobilization and potentially result in increased corn yields compared to those in systems using current conservation agriculture practices. However, this study did reveal that incorporation of cover crop residue in the spring resulted in significantly greater soil inorganic N from the V3 to R2 growth stages in 2016, but the timing of peak soil inorganic N concentrations was similar for both no-tillage and tillage treatments. Similar to soil enzyme activity, soil inorganic N concentration peaks were influenced by soil temperature and weather. The timing of peak soil inorganic N concentration was consistently after the peak potential activity of soil βglucosidase but was similar in timing with potential urease activity. In 2016, the peak β-glucosidase activity for all treatments occurred at the V6 growth stage and urease activity and soil inorganic activity peaked at VT. Potentially due to the rapid warm up in the spring of 2017, both β-glucosidase and urease activities peaked prior to corn planting and the soil inorganic N peak occurred between planting and the V3 growth stage.

times greater relative to 2017. This higher activity in treatments with more available cellulose for decomposition agrees with other cover crop studies that observed increased enzyme activity as a likely result of more biomass (Bandick and Dick, 1999; Mendez et al., 1998). Additionally, a late peak in soil temperature resulted in significantly greater potential soil enzyme activity later in the growing season compared to activity at cover crop termination. However, when the soil temperature peaked early in the growing season, the potential enzyme activity was equal or less at the end of the season compared to activity at cover crop termination. Despite the contrasting precipitation and variation in soil temperature between years, the peak potential soil enzyme activity occurred from early May to the last week in June, similar to timing of peak C input from cover crop residue into the soil. As observed in 2017, late corn planting due to precipitation in April and May could become more common in the Midwest United States (Bartels et al., 2019). Therefore, results from this study, especially from 2017, may be indicative of future trends in soil biology and health as related to increased rainfall that could delay cover crop termination or corn planting. Modeling work has predicted that CR could have a neutral effect on corn yields during simulation periods within increased minimum and maximum temperatures and more variable rainfall (Basche et al., 2016). Soil β-glucosidase and urease activities were also influenced by cover crop and tillage treatment. Specifically, CR-based cover crops increased soil β-glucosidase activity compared to the HV and control treatments at several sampling dates during the decomposition periods, including during peak activity prior to peak inorganic N availability. These CR-based treatments had more biomass available for decomposition after cover crop termination compared to the HV and control in both growing seasons. Greater potential enzyme activities during both decomposition periods in our study due to the presence of CR reflect the patterns of enzyme production by the microbial community of the soil systems as microorganisms increase C acquisition (Allison et al., 2007; Burns et al., 2013). This indicates that higher cover crop biomass levels after termination can influence the metabolic capacity of the soil microbial communities to convert C complexes, such as cellulose complexes found in cover crop residue, to simple sugars. Other studies have shown a similar strong association between soil inorganic N and C cycling enzyme activities, such as soil β-glucosidase activity (Bowles et al., 2014; Piotrowska and Wilczewski, 2012; Sinsabaugh et al., 2005). In 2017, soil β-glucosidase activity was significantly higher in the no-tillage treatments, even though the no-tillage systems had existed for only two years. Other studies have discovered increased soil βglucosidase activity under no-tillage compared to systems that receive tillage (Pandey et al., 2014; Zhang et al., 2014), which is likely a result of an accumulation of residue near the soil surface. However, these studies did not investigate the impact of no-tillage on enzyme activity in the first two years after beginning this conservation agriculture practice. Our findings indicate that fluxes in enzyme activities can be observed in conservation agroecosystems shortly after introducing conservation practices such as cover crops and reduced or no-tillage. Significantly greater potential soil enzyme activity immediately following peak residue decomposition and C release did not translate to greater soil inorganic N concentrations for CR-based treatments. This observation could be attributed to N immobilization by the soil microbial community. In an associated study that characterized the soil microbial community response to the decomposition of cover crop residue using 16S rRNA gene sequencing, there were significant shifts detected in the relative abundance of soil bacteria in the presence of different cover crop species (Nevins et al., 2018). Compared to the HV cover crop, the presence of CR residue resulted in the identification of more cellulolytic bacteria characterizing the difference between the HV and CR microbial communities. This shift in microbial community composition occurred 39 days after cover crop termination and persisted until 109 days after termination, which is equivalent to the V3 and R2 growth stages, respectively, and peak N demand for corn

5. Conclusion Cover crop C release synchronized with corn N demanding growth stages and soil enzyme activity but not peak plant-available N. Carbon release from cover crops was significantly impacted by cover crop species and tillage treatment in both years of this study and cover crop and tillage treatments had a significant impact on soil enzyme activity and inorganic N availability during cover crop decomposition. However, neither cover crop or tillage affected the timing of the soil enzyme activity and inorganic N peaks, but they did impact the magnitude of the peaks. Soil temperature dynamics may have dictated both soil enzyme activity and inorganic N peaks. Cereal rye-based cover crop treatments had significantly higher enzyme activities than HV and controls when enzyme activity was highest; however, greater enzyme activity did not result in greater availability of soil inorganic N. On average, the greatest enzyme activity occurred during the corn growth stages of peak N demand, thus the response of the microbial community to the input of CR C could create a sink for inorganic N that competes with the corn plant. Therefore, this study demonstrates a need to develop adaptive N fertilization management after a winter cover crop with CR that allows to overcome the potential N immobilization during peak corn N demand. Funding This study was supported by the United States Department of Agriculture- Sustainable Agriculture Research and Education Program (SARE) Graduate Student Research Grant GNC16-231 awarded to CJN and SA and Hatch grant IND010811 (SA). Declaration of Competing Interest The authors declare that they have no conflicts of interest. Acknowledgements We thank the Soil Ecosystem and Nutrient Dynamics Lab at Purdue University for assistance with sample collection and lab analyses. The authors thank Drs. Lori Hoagland, Cindy Nakatsu, and Ronald Turco for 8

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guidance on enzyme assays and data analysis. We also thank the research station staff at the Purdue University Agronomy Center for Research and Education for assistance with field plot management. Furthermore, we thank the United States Department of AgricultureNorth Central Region Sustainable Agriculture Research and Education Program (NCR-SARE) for the Graduate Student Research Grant GNC16231 awarded to CJN and SA.

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