REGULAR ARTICLE

Organic amendment effects on potato productivity and qualityare related to soil microbial activity

H. T. Ninh & A. S. Grandy & K.Wickings & S. S. Snapp &

W. Kirk & J. Hao

Received: 31 March 2014 /Accepted: 30 July 2014 /Published online: 12 September 2014# Springer International Publishing Switzerland 2014

AbstractAims Applying manure to row-crop systems can reduceinorganic fertilizer dependence and enhance soil biologyand crop yields. However, it remains unclear whetherlow manure application rates or semi-annual applicationrates can provide these benefits. Our objective was toevaluate the effects of variable rates and timing ofmanure application on soil microbial processes and cropperformance in a potato-corn cropping system.Methods We tested the effects of five manure applica-tion rates of 0.0 (Ctrl), 1.54 (T1), 3.08 (T2), 6.16 (T3),and 12.32 (T4) Mg C ha−1 on potato productivity, se-verity of common scab, and soil biological processes.

Results The highest rates of manure application consis-tently increased crop yields but even the lowest rate(1.54 Mg C ha−1) increased potato and corn yields.The severity of common scab incidence on daughtertubers was reduced by treatments T2, T3, and T4 in yearone but was unaffected by any treatment in year two.Yield increases and reduced common scab severity wererelated to increased activities of C- and N-acquiringenzymes and microbial biomass C and N.Conclusions Manure application rates of <2 Mg C ha−1

can provide crop and soil benefits that appear to increasewith multiple applications, while higher applicationrates provide stronger and more consistent effects on

Plant Soil (2015) 386:223–236DOI 10.1007/s11104-014-2223-5

Responsible Editor: Hans Lambers.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s11104-014-2223-5) contains supplementarymaterial, which is available to authorized users.

H. T. NinhAgricultural Projects Management Board - Ministry ofAgriculture and Rural Development,Hanoi, Vietname-mail: hoangthaininh@gmail.com

A. S. Grandy (*)Department of Natural Resources and the Environment,University of New Hampshire,Durham, NH 03824, USAe-mail: stuart.grandy@unh.edu

K. WickingsDepartment of Entomology, Cornell University, New YorkState Agricultural Experiment Station,Geneva, NY 14456, USAe-mail: kgw37@cornell.edu

S. S. SnappDepartment of Plant, Soil and Microbial Sciences, W.K.Kellogg Biological Station, Michigan State University,Hickory Corners, MI 49060, USAe-mail: snapp@msu.edu

W. KirkDepartment of Plant, Soil and Microbial Sciences, MichiganState University,East Lansing, MI 48823, USAe-mail: kirkw@msu.edu

J. HaoDepartment of Plant, Soil and Environmental Sciences,University of Maine,Orono, ME 04469-5722, USAe-mail: jianjun.hao1@maine.edu

yields, and especially soil biological properties relatedto nutrient cycling and organic matter dynamics.

Keywords Manure . Soil organic matter . Potato .

Enzymes .Microbial biomass . Potato common scab

Introduction

Michigan grows about 17,000 ha of potatoes (Solanumtuberosum L.) annually, more than any other vegetablecrop (MDA 2009). The potato production industries inMI and elsewhere face many agronomic and environ-mental challenges such as declining soil organic matterconcentrations, depressed soil biological activity, andintense pressure from diseases such as stem canker,black scurf, and common scab (Hao et al. 2009; Poet al. 2010; Larkin et al. 2010). Further, N fertilizationat high rates (i.e. ~150 kg N ha−1, Ziadi et al. 2011) toensure an adequate supply in sandy potato soils (Pruntyand Greenland, 1997) can result in high rates of nitrateleaching and nitrous oxide emissions (Honisch et al.2002; Zebarth et al. 2005; Munoz-Arboleda et al.2008). These challenges are common to other potatogrowing regions as well, where declines in soil structur-al stability, biological activity, organic matter concentra-tions, and crop productivity have been frequently re-ported (Grandy et al. 2002; Rees et al. 2002; Carter et al.2003).

Strategic management of soil organic inputs can pro-vide N, promote soil microbial activity, increase plantproductivity (Acosta-Martinez et al. 2007; Larkin et al.2011) and alter the soil physical environment by pro-moting aggregation and reducing bulk density (Celiket al. 2004; Hemmat et al. 2010). In a recent meta-analysis, Kallenbach and Grandy (2011) found a globalaverage increase in soil microbial biomass C and N of36 and 27 %, respectively, in response to organicamendments (animal-based compost or manure) acrossa wide range of cropping systems, soil conditions, andorganic amendment management strategies. Grandyet al. 2002 found that combined applications ofcompost and manure substantially increased soilaggregation and total soil organic matter in Mainepotato cropping systems. Similarly, Moulin et al.(2011) found that compost applications to potato-beanrotations increased soil C concentrations and aggregatestability. Other studies have found that the use of com-post or manure soil amendments increases soil structure

formation (Grosbellet et al. 2011), biological activity(Diacono and Montemurro, 2010), and soil organicmatter concentrations (Pritchett et al. 2011).

One of the primary motivations for using organicamendments is that they may influence soil biologicalfunctions and overall plant health in ways that helpreduce plant disease (Bernard et al. 2014). Potato com-mon scab, caused by multiple species of Streptomyces,with Streptomyces scabies being dominant, is a commontuber disease of potatoes worldwide (Loria et al. 2006).Streptomyces scabies can have a significant impact onmarketable yield by causing corky lesions on the tubersurface (Hao et al. 2009; Wanner and Haynes 2009) andis a long-term production challenge because the patho-gen can survive in the soil and plant debris for more than10 years (Conn and Lazarovits 1999). Streptomycesspecies capable of causing common scab can survivein the soil even under extreme environments such ashigh temperature and a wide range of moisture condi-tions, and produce a phytotoxin, thaxtomin, which in-hibits biosynthesis of cellulose (Wach et al. 2005; Loriaet al. 2006). To date, many studies seeking controls forcommon scab in potato systems have been focused onmaintaining low soil pH; however, this approach is onlymarginally effective in preventing the high crop lossesobserved in many regions (Loria et al. 2006). The use ofmanures and compost have been reported to increase theincidence of common scab on potato tubers (Bailey andLazarovits, 2003) but these results are variable andopposite results have been reported (Conn andLazarovits, 1999).

Growers are using organic amendments to enhancesoil biological activity but there is considerable uncer-tainty about the processes involved and linearity of doseresponse, if any. While many studies have focused onhigh doses (e.g. > 15 Mg C ha−1) that are known toincrease soil organic matter concentrations and biolog-ical activity (e.g. Grandy et al. 2002), they are rarelyeconomical, nor can they be indefinitely sustained be-cause of excessive N and P loading (Carter, 2007; Connand Lazarovits, 1999). Thus, key questions remainabout the extent to which there’s a threshold responseto different amendment application rates, and whetheramendment inputs can be distributed over time andremain effective. Further, variation in the chemistryand composition of organic amendments can stronglyinfluence their behavior in soils, and it remains uncertainwhether poultry manure, which is available in manyagricultural regions, provides the improvements in soil

224 Plant Soil (2015) 386:223–236

quality seen with other animal-based amendments(Kallenbach and Grandy, 2011; Fereidooni et al. 2013;Malik et al. 2013). We evaluate modest application ratesof dried poultry manure, and investigate if higher ratesapplied semi-annually can substitute for annual applica-tion to enhance soil biology and augment plant growth.Our objectives were to examine: 1) effects of variablerates of poultry manure application on potato yields andquality; 2) soil biological responses to manure applica-tion rates and their relationships to crop yield and qual-ity; and 3) whether crop and soil responses to manureapplications persist for longer than a single season.

Materials and methods

Experimental site and crop management

Our study was carried out at the Michigan State Univer-sity Potato Research Farm (MPRS) in Entrican,Montcalm County, Michigan (43°21′13′ N and 85°10′33′ W). The experimental design was a randomizedcomplete block with 5 treatments and 5 replicates. Ex-perimental plots were 3.5 m wide and 7.6 m long with0.9 m between potato rows and 20 cm between seedpieces within rows. The experiment was set up with twophases. The first phase was planted with potato, cv.‘Snowden’, in 2009, and then corn, cv. ‘Great Lakes404163VT3’, in 2010. The second research phase wasplanted with potato, cv. ‘Snowden’, in 2010 (Supple-ment, Table 1), and both phases were irrigated to main-tain soil moisture at field capacity (Supplement Table 2).

Potato plots were amended with dehydrated, pellet-ized poultry manure (C: 45 %, N: 4 %, P2O5: 3 %, K2O:2 %, and Ca: 8 %) in 2009 and 2010, supplied fromHerbruck Poultry Ranch in MI, one of the primarysuppliers to the Michigan potato industry (http://www.herbrucks.com/index.php/products-and-services/dried-fertilizer).Manure was applied prior to planting potatoesin May 2009 (Phase one) and April 2010 (Phase two) atfive rates: 0.0 (Ctrl), 1.54 (T1), 3.08 (T2), 6.16 (T3), and12.32 (T4) Mg C ha−1. In 2010, T1 was the onlytreatment established in 2009 to receive manure priorto corn planting (Phase one). Thus, T1 received twoapplications of 1.54 Mg C ha−1 for a total applicationof 3.4 ton C ha−1 (same total as applied to T2 in 2009).Thus, T1 and T2 can be compared in order to examinethe effect of input timing on crops and soils.

According to grower practices in the region, urea wasapplied three times per year in all treatments to meetproduction needs. Application of inorganic N fertilizerwas in the amount of 150 kg N ha−1 in the control, whilein other treatments inorganic N fertilizer applicationswere reduced based upon estimates that 50 % of themanure N would mineralize in the first year (Supple-ment, Table 3). Although available Nwas expected to behigher in T3 (169 kg N ha−1) and especially T4(263 kg N ha−1), they still received an early season ureaapplication to ensure adequate N supply for potatoeswhen N mineralization rates were expected to be low,following MSU recommendations (Snapp et al., 2002).At planting, urea was applied on all plots at a rate of16 kg N ha−1. The second urea application occurred on24 Jun 2009 at a rate of 67 kgN ha−1 for Ctrl, T1 and T2;and 30 kg N ha−1 for T3. Urea was applied a third timeon 9 Jul 2009 at a rate of 67 kg N ha−1 for Ctrl and33 kg N ha−1 for T1. Potato seed pieces were planted on22 May 2009 and 20 May 2010 into 4 row plots andharvested on 15Oct 2009 and 19Oct 2010, respectively.Potato plants were desiccated 30 d before harvest usingdiquat (Reglone Desiccant) at 2.3 L ha−1 in 200 L H2Oha−1. The center two rows of each plot were harvestedusing a one-row potato harvester to determine tuberyield and size grade. A total of 100 tubers per plot weresampled to assess common scab incidence and severity(described below). Tubers were graded and weighedaccording to USDA market classes: oversize>8.3 cm;A=5.1–8.3 cm; B<5.1 cm in any plane. The grade USNo.1 is the sum of oversize and A potatoes.

Rye was planted after potato harvest for a wintercover crop in all treatments. In Phase 1, the cover cropwas followed by corn in spring 2010. During the cornyear, manure was applied to T1 only, at a rate of 1.54 Cha−1 on 23 Apr 2010. Corn (Great Lakes 404163VT3)was planted on 10 May 2010 and all plots receivedidentical fertilizer applications based on Michigan StateUniversity best management practices for the region.Corn was harvested from the two middle rows of eachplot on 2 Nov 2010 using a one-row corn harvester.

Scab incidence assessment

Scab severity ratings were based on the potato surfacearea infected by scab lesions and whether or not lesionswere pitted (Driscoll et al. 2009): rating value 0=0 %surface area infection; 1=1–10 % surface infection; 2=11–25 % surface infection; 3=26–50 % surface

Plant Soil (2015) 386:223–236 225

infection with 1–5 % of lesions pitted <1 mm; 4 =>50 % surface infection with 6–25 % of lesions pitted>1 mm; and 5 = >50 % surface infection with >25 % oflesions pitted >1 mm.

Soil Sampling and Analysis

In Phase 1 of the experiment, there were a total of 12 soilsampling times in 2009 (potato) and three samplingtimes in 2010 (corn). In Phase 2, soil samples weretaken in potato plots four times over the growing seasonin 2010. Soil samples were taken to a depth of 15 cmwith a 2-cm diameter corer. Twelve replicate sampleswere taken within each plot. Each of the twelve sampleswas taken at a distance of ~15 cm from a plant in orderto capture soil biological and nutrient cycling processesoccurring in the vicinity of the root zone. The twelvesamples were combined to form a composite samplerepresentative of the entire plot. Soil samples were im-mediately put into a cooler containing ice (~4 °C) in thefield then refrigerated at 4 °C until processed. All thesoil samples were homogenized by passing through a4 mm sieve prior to soil biological analyses, which werecarried out within one week from sampling date in thefollowing order: enzyme activities, microbial biomass,inorganicN, and finally soil pH (SeeSupplement Table 4for soil sampling schedule).

Soil pH was determined in water with a soil:waterratio of 1:2 w/v according to Robertson et al. (1999).Gravimetric soil moisture content was determined afterdrying field-moist soil in a 65 °C oven for about 48 h.Ten grams of fresh soil were weighed into a 125 mLflask and then nitrate- and ammonium-extracted in50 mL of 1 M KCl for 30 min on a shaker table. Thesolution was filtered through 125 mm filter paper(Whatman #1) and stored at 4 °C. NO3

−-N concentra-tion in the extracted solution was determined using amodification of the method described by Doane andHorwath (2003). This assay uses vanadium to reduceNO3

− to NO2−, which reacts with sulfanilamide and

N-1-naphthyl-ethylenediamine dihydrochloride to forma pink color that is analyzed in 96 well clear microplatesby a spectrophotometer λ=540 nm (Multiskan Ascent,Thermo Scientific, Hudson, NH). Ammonium (NH4

+-N)was measured bymodifying the method described bySinsabaugh et al. (2000). The principle of this assay is touse salicylate and cyanurate to react with ammonium,forming a green color which is measured on a spectro-photometer at λ=630 nm.

Soil biological measurements

Microbial biomass C and N were measured according tothe fumigation/extraction method (Brookes et al. 1985;Beck et al. 1997; Robertson et al. 1999). Chloroform-fumigated and a subset of non-fumigated control sam-ples were extracted with 60 mL of 0.5 M K2SO4. Ex-tracts were stored at −20 °C before analyzing for totaldissolved organic C and total N with a TOC analyzer(Shimadzu, TOC-VCPH with a TNM-1 nitrogen moduleattached). Microbial biomass C or N was calculated asthe difference between TOC or TN in the samples withand without chloroform, and corrected for microbialbiomass extraction efficiencies (C, 0.45; Joergensen2006; and N, 0.54, Brookes et al., 1985).

Enzyme assays followed previously describedprotocols (Saiya-Cork et al. 2002; Grandy et al.2007; German et al. 2012). Soil (1 g) and 125 mLof 50 mM sodium acetate buffer were combined in a140 mL plastic bottle. The pH of sodium acetatebuffer was adjusted to the average soil pH of all thesamples (6.5) using 0.1 M HCl. The hydrolytic en-zymes β-1,4-glucosidase (BG), β-1,4-N-acetyl-glucosaminidase (NAG), and acid phosphatase(PHOS), 50 μL were analyzed in 96-well black plateswith the fluorescing molecule 4-methylumbelliferone(MUB); for the enzyme tyrosine amino peptidase(TAP), 7-amino-4-methylcoumarin (MC) was addedto wells. Phenol oxidase (PHENOX) was assessed inclear plates with L-3,4-dihydroxyphenylalanine (L-DOPA). Hydrolytic enzyme activities were measuredby a fluorometric analyzer (Fluoroskan Ascent, Ther-mo Scientific, Hudson, NH) while PHENOX wasmeasured using colorimetric methods in a spectro-photometer (Multiskan Ascent, Thermo Scientific,Hudson, NH).

Statistical analysis

Statistical analyses of amendment effects were carriedout with a repeated measure analysis of variance(ANOVA) using Proc Mixed in SAS (SAS version9.2, SAS Institute Cary, NC, USA). A one-wayANOVAwas also used to examine seasonal averages for eachdata set. Assumptions of normality and equal varianceof residuals were examined by Proc Univariate in SASand log transformations were used if necessary to meetthese assumptions. The best fit model was chosen basedon the AIC values for the unequal variance structure

226 Plant Soil (2015) 386:223–236

models. Where ANOVA indicated significant differ-ences, Fisher’s protected LSD (p<0.05) was used toseparate treatment means. Pearson’s correlation coeffi-cients were calculated to examine relationships amongparameters.

Results

Soil Environmental conditions

The daily temperature was collected near the researchsite from 20 Apr to 20 Oct in 2009 and 2010. Thetemperature in 2010 was significantly higher than in2009 (p<0.05), especially during 20 May to 20 Jul(Supplement Fig. 1). The mean temperature over6 months from 20 Apr to 20 Oct was 15.4 °C in 2009and 17.5 °C in 2010 (Source: http://enviroweather.msu.edu). Total precipitation (Supplement Fig. 2) during thegrowing season in 2009 (445 mm) was higher than in2010 (373 mm). However, the higher rainfall in 2009was driven by a few large precipitation events; themedian rainfall in 2009 (3.0 mm d−1) was lower thanmedian rainfall in 2010 (4.6 mm d−1) and the number ofrainy days was the same for both years (65 days). Inboth years, fields were irrigated six times (SupplementTable 2); however, more water was applied in 2010leading to a higher amount of irrigation water used thatyear. Manure application significantly affected soilmoisture in the potato system in 2009 but not in 2010(Fig. 1). In 2009, the soil moisture in T2 (11.7±0.5 %)and T4 (12.0±0.3 %) was higher than in Ctrl (10.0±0.4 %). In the corn soil in 2010, the moisture content in T4(9.9±0.2 %) was significantly higher than the othertreatments, which were similar to each other (8.1±0.5 %).

Yields and potato common scab

Manure application had a positive effect on potatoproductivity, increasing total potato yields (20 %,17 %) and the yield of grade US No.1 potatoes(30 %, 25 %) in T3 and T4, respectively, relative toCtrl (Table 1). In 2010, manure increased totalyields (T1:17 %, T2:23 %, T3:23 %, andT4:36 %) and US No.1 potato yield (T1:18 %,T2:22 %, T3:27 %, and T4:36 %) relative to Ctrl.T4 produced the highest total yield in all the sys-tems (38.7 Mg h−1). T3 and T4 also produced more

overweight potatoes than other treatments. Therewas no difference in B grade potato yield betweenany of the systems in 2010. In 2009, the severity ofcommon scab in the Ctrl treatment did not differfrom that of T1 and T2, but was higher than that ofT3 and T4 (Fig. 2). Scab severity in T4 (2.8) waslower than in T1 (3.5) and T2 (3.3). In 2010,common scab severity was lower than in 2009and there were no differences between treatments.

Although the manure applications were madeonly in 2009 to all treatments but T1, whichreceived manure both years, they still influencedcorn yield in 2010 (Fig. 3). Corn yield was higherin T4 (14.1 Mg ha−1), T2 (13.2, Mg ha−1), and T1(13.3, Mg ha−1) than in Ctrl (11.8 Mg ha−1),which was similar to T3 (12.6, Mg ha−1). Cornyield in T1 was not different from T2, T3 and T4,and the yield in T4 was significantly higher thanin T2 and T3.

aab

bbcc

b

a

Fig. 1 Organic amendment effects on average soil moisture (%)over the growing season from Apr to Sep in soil taken from potatoplots during a; Phase 1, 2009 and b; Phase 2, 2010. Manure wasapplied at five rates: 0.0 (Ctrl), 1.54 (T1), 3.08 (T2), 6.16 (T3), and12.32 (T4) Mg C ha−1 prior to planting potatoes. Means withdifferent letters are significantly different (p<0.05)

Plant Soil (2015) 386:223–236 227

Soil pH and inorganic N

In 2009, the seasonal average pH in all manuretreatments was higher than in Ctrl (5.85±0.03),while pH in T3 (6.58±0.05) and T4 (6.79±0.07)were also higher than in T1 (6.22±0.03) and T2(6.13±0.08). In 2010, the average soil pH in T2(6.13±0.19) was higher than in Ctrl (5.84±0.14)but lower than T3 (6.55±0.08) and T4 (6.54±0.11). In 2009, seasonal average NO3

−-N concentra-tions were similar in Ctrl and T1, but the higherrates of manure application in T2, T3, and T4 in-creased NO3

−-N concentrations (Table 2; Supple-ment Fig. 3). NO3

−-N in T4 was higher than in T2and T3, which did not differ from one another. In2009, average seasonal soil NH4

+-N concentrationswere higher in all the manure treatments than inCtrl. In 2010, manure applications in T2, T3 andT4 increased NO3

−-N relative to Ctrl (Table 2). Theaverage NH4

+-N contents across all treatments in2010 were different from the average NH4

+-N con-tents in 2009. In 2010, the NH4

+-N content in T4was higher than in the remaining treatments, whichdid not differ from one another. Similar to 2009,NH4

+-N concentrations in 2010 declined in Jul.The poultry manure applied in 2009 still influencedcorn soil pH in 2010, with the pH in Ctrl (6.31±0.08), lower than in T1 (6.53±0.07), T2 (6.61±0.07), T3 (6.93±0.06), or T4 (6.97±0.05). Averagedover the growing season, NO3

−-N in T1, T3, and T4were significantly higher than Ctr.

Table 1 Potato Yield responses to manure amendments

2009 B A Overweight US#1 Total yield

Potato yields, Mg ha−1

Ctrl 5.7ab 22.4c 1.2ab 22.8c 28.6b

T1 6.4a 24.6abc 0.2b 24.8bc 31.3ab

T2 5.6abc 23.1bc 1.2ab 24.3bc 29.9b

T3 4.4c 27.4a 2.4a 29.8a 34.2a

T4 4.7bc 26.4ab 2.2a 28.6ab 33.3a

p value 0.022 0.035 0.024 <0.001 0.024

2010

Ctrl 5.7 22.5c 0.4b 22.8c 28.5c

T1 5.6 27.2b 0.8ab 27.9b 33.5b

T2 6 27.9ab 1.2ab 29.1b 35.1b

T3 4.4 28.5ab 2.1a 30.6ab 35.0b

T4 5.7 31.0a 2.0a 33.0a 38.7a

p value ns 0.012 0.026 0.005 0.003

Means for the same tuber size with the same letter are not signif-icantly different (p<0.05)

b

a

aa ab

abb

Fig. 2 Potato scab severity in year 1 (a; Phase 1, 2009) and year 2(b; Phase 2, 2010) at the Montcalm Research Farm in response toorganic amendments. Manure was applied at five rates: 0.0 (Ctrl),1.54 (T1), 3.08 (T2), 6.16 (T3), and 12.32 (T4) Mg C ha−1 prior toplanting potatoes. Means with different letters are significantlydifferent (p<0.05)

aab

bcb

c

Fig. 3 Organic amendments effects on average corn yield (mean±SE, 103 kg ha−1) in Phase 1, 2010. In 2009, manure was appliedat five rates: 0.0 (Ctrl), 1.54 (T1), 3.08 (T2), 6.16 (T3), and 12.32(T4) Mg C ha−1 prior to planting potatoes. In 2010, additionalmanure was added to T1 (3.08 Mg C ha−1) prior to corn planting.Means with different letters are significantly different (p<0.05)

228 Plant Soil (2015) 386:223–236

Tab

le2

InorganicNresponsesto

compostsoilam

endm

entsin

potato

andcorn

soils.a

NO3− -N

NH4+-N

Potato

2009

Date

Ctrl

T1

T2

T3

T4

pvalue

Date

Ctrl

T1

T2

T3

T4

pvalue

2-Jun-09

3036

32.6

32.8

39.8

ns2-Jun-09

20.3d

48.9

cd70.3bc

102.1b

150.9a

0.0003

18-Jun-09

5.78b

5.72b

8.06b

53.3a

30.5a

<0.0001

18-Jun-09

17.8c

46.1ab

18.1c

36.9bc

59.2a

0.0154

1-Jul-09

5.05c

8.42b

16.8a

23.3a

17.1a

<0.0001

16-Jul-09

0.71c

1.69b

1.77b

1.38b

2.35a

0.0001

16-Jul-09

38.2b

38.3b

54.6b

48.2b

87.0a

0.0034

29-Jul-09

0.53d

0.62

cd0.76bc

0.93b

1.82a

0.0001

29-Jul-09

17.2c

20.5c

31.6ab

24.9bc

44.3a

0.0036

13-A

ug-09

1.03c

1.27bc

1.73b

1.78b

2.64a

0.0001

24-A

ug-09

5.58b

6.07b

9.44a

7.69ab

9.25a

0.0286

24-A

ug-09

1.40b

1.52b

1.78ab

1.95a

2.15a

0.0013

9-Sep-09

10.9c

12.2bc

14.9ab

8.80d

15.6a

<0.0001

9-Sep-09

1.42

1.31

1.22

1.28

1.37

ns

23-Sep-09

15.7b

16.4b

20.4ab

17.9b

26.1a

0.0094

23-Sep-09

0.87b

1.04b

0.69b

1.39a

1.67a

0.0002

13-O

ct-09

1.91c

2.36c

4.44b

6.08ab

6.48a

<0.0001

13-O

ct-09

1.04bc

0.88c

1.05bc

1.30ab

1.58a

0.0012

26-N

ov-09

3.15

3.2

4.65

3.57

4.03

ns26-N

ov-09

0.76

0.79

0.68

1.03

0.8

ns

Potato

2010

1-Jun-10

18.8d

25.1

cd34.2bc

44.6b

90.0a

<0.0001

1-Jun-10

26.4bc

25.3bc

23.4c

34.4b

51.2a

0.0012

5-Jul-10

26.2

31.2

31.5

30.2

35.7

ns5-Jul-10

3.81a

4.05a

3.26a

1.39b

1.08b

0.0027

12-A

ug-10

4.50c

7.05b

7.74b

7.08b

13.0a

<0.0001

12-A

ug-10

1.04a

0.41b

0.52b

0.49b

1.69a

0.0005

14-Sep-10

8.60c

13.3c

22.2b

27.5a

29.7a

<0.0001

14-Sep-10

0.47ab

0.33b

0.43ab

0.55a

0.70a

0.0417

Corn2010

24-M

ay-10

4.56c

11.8a

5.77bc

6.10b

7.05b

<0.0001

24-M

ay-10

0.64

0.7

0.69

0.77

0.79

ns

19-Jul-10

4.69bc

4.56bc

3.53c

6.74a

6.05ab

0.0107

19-Jul-10

4.88a

1.69b

1.41b

4.30a

2.47b

0.0002

29-Sep-10

2.57c

3.56ab

3.40b

4.24ab

4.44a

0.0076

29-Sep-10

0.24b

0.32ab

0.24b

0.39a

0.38a

0.0362

Average

3.92c

6.81a

4.30c

5.65b

5.82b

<0.0001

Average

1.93a

0.90b

0.78b

1.82a

1.08b

<0.0001

Mean±SE

(mgNkg

-1soil)

Means

with

thesamelettersdidnotd

iffersignificantly

(p<0.05).Abbreviation:

ns–notsignificant

Plant Soil (2015) 386:223–236 229

Microbial biomass

There were differences in microbial biomass C (MBC)and N (MBN) between treatments over the growingseason (Table 3). Manure additions with the exceptionof T1 increased MBC. All five measurements of MBCin 2009 showed a treatment effect. In Phase 2 potato,2010, the seasonal average MBC in T1 and Ctrl did notdiffer and were lower than the other treatments. Onlythree measurements were taken in 2010 but each ofthese exhibited a strong treatment effect (p<0.0001)and showed that higher amendment application ratesgenerally increased MBC (Table 4). T4 had the highestMBC on all dates sampled.

Seasonal average MBN in 2009 was differentamong the treatments (Table 3). MBN in T2, T3,and T4 were higher than in Ctrl. MBN in T3 and T4did not differ, and was about a fold higher thanMBN in Ctrl. There was variation among dates intreatment effects on MBN. For example, on the firstand the last dates, MBN in T4 was not differentfrom that in Ctrl but at three other dates MBN washigher in T4. In 2010, the seasonal average of MBNwas again related to amendment application rate.The MBN values of T1 and T2 did not differ fromone another, or from Ctrl on 12 Aug 2010; however,

on the next measurement, 14 Sep 2010, MBN in allthe manure treatments were higher than in Ctrl. Incorn soil, higher seasonal average MBC and MBNin each of the manure treatments than Ctrl showedthe persistent effects of manure applications theprevious year.

Enzyme activities

In 2009, average BG activities in T2 and T4 were higherthan in Ctrl (Fig. 4; Supplement Figs. 4, 5 and 6) buttreatment differences varied across dates. For example,on 16 Jul 2009, BG in T2 and T4 were higher than inCtrl and in T1. At the next measurement on 29 Jul 2009,only BG in T2 was higher than in Ctrl. In 2010, averageseasonal BG activity in T4 was higher than in T1, T2,and T3 but similar to that of Ctrl. The manure applica-tion rate did not affect BG activity in potato soils in2010 at the 2 first dates, but on 12 Aug 2010 and 14 Sep2010, BG in T4 was not different from Ctrl but washigher than the 3 other manure treatments (Fig. 4; Sup-plement Figs. 4, 5 and 6).

The seasonal average NAG activity was significantlyaffected by manure application rates in 2009. NAGactivities in T2, T3 and T4 were higher than in Ctrland were higher in T2 and T4 than in T1 and T3. On 2

Table 3 Microbial biomass C and N responses to organic amendments

Treatment Phase 1: Potato 2009 Phase 1: Corn 2010 Phase 2: Potato 2010

1-Jul-09 29-Jul-09

13-Aug-09

9-Sep-09

26-Nov-09

24-May-10

19-Jul-10

29-Sep-10

11-Jun-10

12-Aug-10

14-Sep-10

microbial biomass C mg kg−1 soil

Ctrl 45.1bc 155.5ab 134.3b 70.7c 103.6b 51.2b 91.9c 60.9d 69.6d 79.6c 73.3c

T1 37.8c 205.5a 139.5b 69.0c 110.1b 51.2b 136.8ab 77.7bc 67.3d 74.4c 76.9c

T2 32.8c 169.5ab 215.5a 84.9bc 132.5ab 139.1a 140.9ab 86.5ab 127.6c 95.0bc 83.8bc

T3 61.3b 203.7a 119.1b 134.0ab 141.8a 123.8a 128.3b 73.1c 155.2b 118.1b 95.4b

T4 128.4a 119.6b 206.9a 148.6a 55.7c 132.4a 157.4a 94.1a 193.5a 176.9a 137.7a

p value < 0.0001 0.0275 0.0009 0.015 < 0.0001 < 0.0001 < 0.0001 0.0001 < 0.0001 < 0.0001 < 0.0001

microbial biomass N mg kg−1 soil

Ctrl 18.1bc 18.1b 19.3b 9.75c 16.6c 13.0b 17.4b 8.3d na 12.8c 11.7d

T1 11.9c 21.9b 28.3b 17.7bc 17.5bc 12.6b 23.5a 12.1c na 16.7c 18.6bc

T2 25.9ab 24.7b 19.7b 16.9bc 21.7ab 22.6a 25.3a 14.9ab na 16.6bc 16.5c

T3 34.9a 37.2a 19.8b 35.0a 26.a 21.9a 24.3a 13.2bc na 20.8b 21.3b

T4 23.7ab 46.9a 46.2a 23.5ab 21.1abc 27.1a 27.2a 16.2a na 32.2a 35.4a

p value 0.0125 0.003 0.0001 0.0082 0.0167 0.0012 0.0471 < 0.0001 na < 0.0001 < 0.0001

230 Plant Soil (2015) 386:223–236

Jun 2009, NAG activity in T4 was three times higherthan in Ctrl. SeasonalmeanNAG activities in 2010weresimilar to those in 2009 (Fig. 4). NAG activities were

similar across sampling dates in T3 and T4 were higherthan in Ctrl and typically those in T1 and T2 weresimilar to those in Ctrl, except on 1 Jun 2010.

Table 4 Pearson’s correlation coefficients (r) between seasonal means of soil variablesand crop productivity in potato and corn systems

Potato-2009 Total yield Scab W% pH NO3− NH4

+ MBC MBN BG NAG TAP PHOS

Scab −0.56W% 0.39 −0.43pH 0.52 −0.51 0.33

NO3− 0.22 −0.47 0.66 0.68

NH4+ 0.26 −0.48 0.42 0.87 0.82

MBC 0.62 −0.32 0.48 0.64 0.42 0.48

MBN 0.50 −0.59 0.51 0.78 0.74 0.70 0.57

BG 0.35 −0.17 0.77 0.28 0.47 0.32 0.53 0.29

NAG 0.33 −0.39 0.72 0.51 0.64 0.54 0.51 0.46 0.87

TAP 0.45 −0.45 0.77 0.68 0.74 0.66 0.72 0.65 0.80 0.89

PHOS −0.01 −0.11 0.65 −0.19 0.23 −0.05 0.13 0.03 0.76 0.62 0.52

PHENOX 0.10 −0.28 0.16 0.01 −0.04 0.13 −0.06 0.12 −0.09 −0.06 −0.07 −0.11Potato-2010

Scab 0.14

W% −0.17 −0.18pH 0.54 0.30 −0.03NO3− 0.53 −0.15 0.38 0.46

NH4+ 0.35 −0.12 0.19 0.32 0.75

MBC 0.53 −0.01 0.34 0.62 0.91 0.73

MBN 0.61 0.07 0.32 0.61 0.82 0.69 0.91

BG −0.03 0.04 0.36 0.24 0.35 0.38 0.49 0.50

NAG 0.46 −0.04 0.41 0.43 0.89 0.76 0.91 0.87 0.49

TAP 0.53 0.05 0.42 0.62 0.85 0.66 0.92 0.91 0.42 0.89

PHOS −0.22 −0.27 0.52 −0.58 0.31 0.21 0.19 0.10 0.16 0.37 0.19

PHENOX −0.45 0.13 0.11 −0.33 −0.08 0.16 −0.02 −0.02 0.31 0.05 −0.16 0.32

Corn-2010

W% 0.45 .

pH 0.36 . 0.37

NO3 0.36 . 0.32 0.24

NH4 −0.53 . −0.26 −0.13 −0.14MBC 0.51 . 0.53 0.68 0.22 −0.40MBN 0.54 . 0.62 0.70 0.34 −0.34 0.92

BG 0.05 . 0.52 −0.10 −0.04 −0.21 0.35 0.31

NAG 0.32 . 0.49 −0.15 0.12 −0.51 0.32 0.31 0.79

TAP 0.00 . 0.28 −0.43 −0.26 −0.09 0.09 0.09 0.66 0.57

PHOS 0.01 . 0.24 −0.65 −0.11 −0.18 −0.04 −0.07 0.67 0.61 0.79

PHENOX −0.11 . −0.09 −0.42 −0.56 0.03 −0.29 −0.36 0.17 0.15 0.39 0.33

W%, soil gravimetric water content;MBC microbial biomass C,MBN microbial biomass N, BG, β-1,4-glucosidase, NAG, β-1,4-N-acetyl-glucosaminidase, TAP tyrosine amino peptidase, POS acid phosphatase, PHENOX phenol oxidase Bold numbers indicate significance atp<0.05

Plant Soil (2015) 386:223–236 231

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Fig. 4 Organic amendment effects on soil enzyme activities inrotation Phase 1 (planted to potatoes in 2009 and corn in 2010) androtation Phase 2 (planted to potatoes in 2010). Manure was appliedat five rates: 0.0 (Ctrl), 1.54 (T1), 3.08 (T2), 6.16 (T3), and 12.32

(T4) Mg C ha−1 prior to planting potatoes in 2009 (phase 1) and2010 (Phase 2). In 2010, additional manure was added to T1(3.08 Mg C ha−1) prior to corn planting

232 Plant Soil (2015) 386:223–236

Average PHOS activity in T2 was higher than inother treatments in 2009 (Fig. 4), almost two-fold higherthan in Ctrl and T3, although differences varied acrossthe dates. Average annual PHOS activities in 2010 werenot different among treatments but on 1 Jun 2010,PHOS activity in T1 was higher than Ctrl, and on 5Jul, PHOS activity in T3 was lower than in all theremaining treatments.

In 2009, seasonal average TAP activities in all themanure treatments were higher than in the Ctrl, and TAPactivity in T2, T3, and T4was higher than in T1. In 2010as in 2009, TAP activities were higher in all manuretreatments than in Ctrl. In 2009, average PHENOXactivities in Ctrl and T1 were higher than in T3, andhigher in T4 than in T2 and T3. In 2010, averagePHENOX activity in Ctrl was higher than in T1, T2,and T3, although this was primarily driven by signifi-cant effects on 14 Sep 2010 (Fig. 4; Supplement Figs. 4,5 and 6).

In corn soil in 2010, there were no treatment maineffects or treatment by time interactions for BG or NAG(Fig. 4). Averaged over the season, TAP activity in T1,T2 and T4 were not different from Ctrl which washigher than in T3. The seasonal average PHOS activityin T3 was lower than in Ctrl, T1 and T2. PHOS activityin T2 did not differ from T1, and was higher than in T3and T4. PHENOX was measured only once in thebeginning of the season and did not show any treatmenteffect.

Pearson’s correlation coefficients between variablesalso indicated that potato yield in 2009 was negativelycorrelated to common scab and positively correlated topH, microbial biomass C and N, and TAP enzymeactivity (Table 4). The potato yield in 2010 was

positively correlated to pH, NO3−-N, microbial biomass

C&N, and NAG and TAP enzyme activities, and nega-tively correlated to PHENOX enzyme activity; therewas no correlation with common scab.

Discussion

We found that poultry manure application increasedpotato yield, with higher rates of manure producinghigher yields, primarily of US No.1 tubers. These resultsare consistent with an earlier investigation of potatoresponses to manure conducted in Michigan (Nyiranezaand Snapp, 2007), while the majority of other studiesshowing comparable increases in potato yields follow-ing manure applications used higher application rates(Mallory and Porter 2007; Larkin and Tavantzis, 2013;Bernard et al. 2014). While there have been concernsabout organic matter inputs increasing scab severity dueto its effects on pH andwater availability, during the firstyear of this study all manure treatments except T1reduced common scab severity, whereas in 2010 therewas no effect of manure application on PCS. Changes insoil biological activity and physical and chemical char-acteristics associated with application of poultry manuremay have influenced PCS severity, but disease inci-dence, yields, and soil biological activity showed vari-able responses to application of manure across yearspointing to complex interactions between management,soil properties, and environment. Interestingly, a com-prehensive survey of soil properties and Verticilliumwilt incidence on hundreds of potato fields hashighlighted similarly complex relationships amongplant and soil biogeochemical properties, with soil

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Fig. 4 (continued)

Plant Soil (2015) 386:223–236 233

organic matter the most consistent property associatedwith healthy potato tubers (Davis et al., 2001).

The highest rates of poultry manure application inthis study consistently enhanced soil enzyme activities,microbial biomass and nutrient availability. These re-sponses were likely due to increases in the availability oforganic substrates that drive microbial activity (Grandyet al. 2002; Larkin et al. 2010). The availability ofsimple organic N-bearing compounds abundant in thepoultry manure may be particularly important. Grandyet al. (2009) showed that the activities BG, NAG and L-leucine aminopeptidase (LAP), all enzymes producedby microbes to degrade carbohydrates, were highlycorrelated to the abundance of N-bearing compounds.Consistent with this, we found that the enzymes BG,NAG, and TAP, as well as microbial biomass and inor-ganic N, appeared to be related to substrate availabilityfrom poultry manure. There was no correlation betweenPHOS and MBC, N, or inorganic N, likely becausePHOS can be produced by a wide range of taxa and inresponse to varying environmental conditions(Sinsabaugh et al. 2008).

While large organic amendment applications are ex-pected to change soil biological processes, it’s unclearwhether smaller applications can impact soils, whichtypically contain~30–100 Mg C ha−1 in the surfacehorizon. Soil responses to T1 (1.54 Mg C ha−1) weremodest but TAP activity increased in 2009 and 2010,and phenol oxidase activity decreased in 2010. Therewere also temporally inconsistent increases in microbialbiomass after two years of application. Thus, short-termand relatively small amendment applications can altersoil biological processes and nutrient cycling, eventhough total soil C will likely take much longer torespond. Further, T1 increased corn yield to equal thatof T2 and T4 in 2010. Crop yield may not benefit fromlow rates of manure in the short term but may beincreased by the accrual of nutrients supplied by multi-ple applications of small amounts of manure (Evanyloet al. 2008). Smaller applications may also minimizenutrient losses and thus increase nutrient availabilitywhile minimizing the negative environmental impactsof using higher rates of organic amendments (Munoz-Arboleda et al. 2008; Bowden et al. 2010). Althoughvery high rates of organic matter additions may optimizeyields in the short term (e.g. > 20Mg ha−1; Grandy et al.2002; Smiciklas et al. 2008) such rates are not econom-ical and long-term will often result in excessive P- andN-loading.

Our results suggest that environmental conditionsand inherent site properties influence crop and soil re-sponses to organic amendments (Bernard et al. 2014).For example, potato scab varied among organic amend-ment treatments in 2009 but not in 2010. The differencein overall response between years may have been due todifferences in meteorological factors such as precipita-tion, especially early in the season during tuber initiationand early development, which accentuated treatmenteffects on soil biological and chemical properties thatinfluence common scab. 2009 was a wetter and cooleryear, and scab severity was negatively correlated withsoil moisture content, pH, measures of soil N availabil-ity, and N-acquiring enzymes (TAP). Further, differ-ences in soil moisture among treatments in 2009 mayhave influenced the activity of antibiotic-producing bac-teria that inhibit Streptomyces spp. in soil (Kinkel et al.1998; Meng et al. 2012). Thus additional but not exces-sive water availability in manure-amended soils in 2009,along with greater C substrate availability, may havepromoted a more biologically active, suppressive soiland a healthier potato crop.

The strong crop and soil responses to even low ratesof organic amendments in these sites also likely reflectsite conditions and history (Bernard et al. 2014). Organ-ic matter concentrations at MPRS soils are low and tothe best of our knowledge the manure applications inthis study were the first made to this site. After years ofpotato production and low organic matter inputs to thesesandy soils, microbes likely responded to manure appli-cations, even the lowest rates, because they are severelyC limited, with only a fraction of the total C likelyavailable for microbial activity. Laboratory studies showthat microbes respond to minute C additions (μg g-1; DeNobili et al. 2001) while rhizosphere C inputs of<mg g−1 are known to directly accelerate microbial activ-ity and lead to priming effects. Thus we should expect –and not be surprised – that T1 would have some effecton microbial activity given C inputs amount to~0.8 mg g−1, comparable to reported rates of rootexudation.

Conclusion

Carter et al. (2004) argued that an annual manure appli-cation rate of 2–3 Mg C ha−1 was the minimum amountneeded to maintain soil organic matter levels in potatosystems. In another study of potato rotations (Angers

234 Plant Soil (2015) 386:223–236

et al. 1999), crop residue inputs higher than 2.4 Mg Cha−1 yr−1 possessed the capacity to maintain organicmatter levels in the soil. Our results suggest that theremay be accelerated microbial activity and yield benefitsfrommanure application rates as low as 1.54MgC ha−1;further, T1 influenced microbial biomass and TAP ac-tivity in corn soils, suggesting that the benefits of verylow rates of application may accumulate over time.Thus, if economic limitations prevent higher applicationrates, and when there are concerns about nutrientoverloading, those below 2.0 Mg C ha−1 can providebenefits including enhanced microbial activity thatcould increase over time; for stronger and more consis-tent effects on yields, and especially on soil biologicalproperties related to nutrient cycling and organic matterdynamics, higher application rates are recommended.

Acknowledgments We appreciate the support for this workprovided by the Michigan Agricultural Experiment Station andthe Vietnamese Agricultural Technology Project, ADB.Herbruck's Poultry Ranch supplied the manure used in this study.

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