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Applied Soil Ecology
journal homepage: www.elsevier.com/locate/apsoil
Perennial crop legacy effects on nematode community structure in semi-arid
wheat systems
Andy Burkhardta,⁎, Shabeg S. Briarb, John M. Martina, Patrick M. Carrc, Jennifer Lachowieca,
Cathy Zabinskid, David W. Robertse, Perry Millerd, Jamie Shermana
a Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT, USA
bOlds College Centre for Innovation, Olds, AB, Canada
c Central Agricultural Research Center, Montana State University, Moccasin, MT, USA
dDepartment of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, USA
e Department of Ecology, Montana State University, Bozeman, MT, USA
A B S T R A C T
The effects of diversifying wheat-based cropping systems in the Northern Great Plains (NGP) on soil chemical and physical properties is well documented: better soil
tilth, improved water infiltration, and higher soil organic matter with crop rotations. However, the impact of crop rotations on soil biology is not as well understood.
Nematode communities reflect soil quality and are directly observable, readily quantifiable, and occupy most of the consumer trophic levels in the soil food web.
Within more humid climates, the community structure is better characterized to make associations with soil health and crop management strategies, but little is
known about their community structure in semiarid regions such as the NGP. For this study, soils under contrasting cropping systems were sampled in the 15th year
of a long-term study to quantify and assess the nematode community. Prior to planting, wheat-chemical fallow had a higher total nematode population than that of
wheat-tilled fallow (P < 0.05). A wheat-pulse system with a history of crop perennation had a greater abundance of uncommon, omnivorous nematodes than a
wheat-pulse system without a prior history of crop perennation. However, plant parasitic nematodes also were higher in abundance under the converted perennial
system. Our results suggest that reducing soil disturbance and including a perennial component to cropping systems will foster a more diverse and balanced nematode
community under semiarid dryland conditions, but potentially at the expense of increased plant parasitic nematode pressure.
1. Introduction
Research over several decades has focused on intensifying and di-
versifying rotations and reducing fallow acres in the Northern Great
Plains (NGP), a region comprised of all or part of Montana, Nebraska,
Wyoming, North Dakota, and South Dakota in the U.S., along with the
Prairie Provinces of Canada (Padbury et al., 2002). The NGP is char-
acterized by a harsh climate with strong fluctuations in weather
(Peterson, 1996). Within Montana, crop production is dominated by
cereals and, increasingly, pulse crops (National Agricultural Statistics
Service, 2018).
The Conservation Reserve Program (CRP), a cost-share and rental
program where farmers are paid by the USDA Farm Service Agency to
set aside cropland in perennial cover to reduce soil erosion, comprised
14 million hectares at its peak across the USA. In Montana, peak CRP
area totaled roughly 1.4 million hectares in 2006 (Barbarika, 2007). By
2017, fewer than 530,000 ha of CRP remained in the state (Barbarika,
2017). This decline in CRP enrollment in Montana can be attributed to
two events: high commodity crop prices in the late 2000s (McBride,
2017), and steadily decreasing land rental payments from CRP
contracts, causing many producers to rethink the economic viability of
their CRP acres. However, the inclusion of a perennial phase to crop-
ping systems can increase soil carbon (C) in integrated crop-livestock
systems (Acosta-Martínez et al., 2010), soil biopore density in fodder
crops (Han et al., 2015), and soil N while improving weed control
during transition to organic wheat production (Borrelli et al., 2015).
Adoption of no-till and reduction of fallow became prevalent across
much of the NGP prior to the reduction of CRP (Tanaka et al., 2010).
The benefits of no-till and elimination of fallow are well documented in
this region (Cutforth and McConkey, 1997; Cutforth et al., 2002; Engel
et al., 2017; Nielsen et al., 2005), and multiple studies show the positive
impact of no-till and annual cropping to soil fungal and microbial
communities (Ellouze et al., 2013; Helgason et al., 2010; Sharma-
Poudyal et al., 2017; Stromberger et al., 2007; Stromberger et al.,
2011). Therefore, adoption of these practices could potentially benefit
farmers in yield-limited dryland environments with positive impacts to
soil physical, chemical, and biological properties.
Describing soil food webs, such as those of nematodes, has become a
way to assess soil function and potential for ecosystem services
(Chertov et al., 2017; Morriën, 2016; Olena et al., 2017; Rousk, 2016;
https://doi.org/10.1016/j.apsoil.2018.12.020
Received 24 August 2018; Received in revised form 28 December 2018; Accepted 29 December 2018
⁎ Corresponding author.
E-mail address: apburkha@gmail.com (A. Burkhardt).
Applied Soil Ecology 136 (2019) 93–100
Available online 05 January 2019
0929-1393/ © 2018 Published by Elsevier B.V.
T
Zhang et al., 2017). Nematode communities are sensitive to dis-
turbances within their environment and are used as indicators of soil
quality (Briar et al., 2007a,b; Briar et al., 2011; Briar et al., 2012; Neher
and Olson, 1999; Yeates and Bongers, 1999). Nematode taxa differ in
their life-history strategies. r-Strategists typically have high fecundity,
small body size, short life cycles, and are tolerant to disturbances; while
K-strategists typically have low fecundity, long life cycles, larger body
size, and are intolerant of disturbance (MacArthur and Wilson, 1967).
The colonizer-persister (cp) value of a nematode life history strategies:
low rank nematodes (cp 1 and 2) behave more as r-strategists; while
those with a high cp value (3–5) follow more of a K trajectory (Bongers,
1990). High cp value nematodes indicate that the soil food web is in a
mature and stable state, while a soil dominated by low cp value ne-
matodes indicate a disturbed and degraded food web.
Soil nematode communities are also classified based on the pre-
valence of stress tolerant, r-strategist nematodes, using the Basal Index;
on the abundance of bacterivore and fungivore nematodes responding
nutrients and resources in the soil, applying the Enrichment Index; on
the abundance of high cp value, K-strategist nematodes that are sensi-
tive to disturbance, with the Structure Index; and on the weighted
average of the cp value of the whole nematode community, using the ∑
Maturity Index (Bongers, 1990, 1999; Bongers and Bongers, 1998;
Ferris et al., 2001; Freckman and Ettema, 1993; Yeates et al., 1993).
Subsets of the nematode community are also described, for example,
the Maturity Index gives a weighted average of the cp value for the free-
living (non-herbivorous) nematode community, and the Plant Parasitic
Index gives a weighted average of the cp value of the plant parasitic
nematode (PPN) community. The Maturity Index, ∑Maturity Index, and
Plant Parasitic Index are all indicators of the progression and diversity
of the nematode community in terms of environmental stress and soil
quality (Bongers, 1990, 1999; Bongers et al., 1995). The metabolic
footprint family of indices provides a quantified measure of ecosystem
services provided by each functional nematode guild by way of quan-
tifying C respiration (Ferris, 2010).
Multiple studies have focused on how these quantitative measures
of the nematode community change in the face of crop management.
Carbon-rich organic fertilizers buffered soil resiliency by increasing
species richness and total abundance (Liu et al., 2016). Conversely,
application of N-rich fertilizers (both organic and inorganic sources)
decreased species richness, species diversity, Maturity Index, and
Structure Index, but increased the abundance of PPNs and enrichment
opportunist microbivores. Just a single year of tillage decreased di-
versity of nematode communities (Berkelmans et al., 2003). Our ob-
jective was to determine long-term effects of tillage and cropping
system on the nematode community structure in wheat-based cropping
systems under dryland management in Montana.
2. Materials and methods
2.1. Study site and experimental design
The trial area is located at the Montana State University Arthur H.
Post Research Farm 7 km west of Bozeman, MT. The soils of the Post
Farm (1474m asl) are Amsterdam-Quagle silt loam soils (fine-silty,
mixed, superactive, frigid Typic Haplustolls) (Soil Survey Staff, 2017).
The field was transitioned to no-till in 2000 and the rotation study was
established in 2002. On 1 May 2017, the soil water profile was at field
capacity to a depth greater than 1.2m (data not shown) and further
Fig. 1 shows precipitation and average daily temperature for the Arthur
H. Post Farm for 2017.
Eight cropping systems were compared to determine the impact of
dryland cropping systems on soil nematodes. The systems included
wheat-tilled fallow, wheat-chemical fallow, continuous wheat, wheat-
pulse grain, wheat-pulse forage (pulses harvested for forage), wheat-
pulse manure (pulses terminated with herbicide at first bloom), organic
wheat-pulse, and wheat-pulse grain (previously alfalfa-grass mix to
mimic Conservation Reserve Program (CRP) from 2003 to 2012). The
cropping systems were established in 7.6 m by 22.9 m plots in a ran-
domized complete block design with cropping system treatments re-
plicated four times. All systems except wheat-tilled fallow and organic
wheat-pulse were managed under no-till practices. Table 1 includes a
description of the crop sequence and cumulative applied nitrogen (N)
fertility for each cropping system from 2003 to 2017.
Nitrogen fertility was managed so 50 kg N ha−1 Mg grain−1 was
available at wheat planting in all cropping systems. Fertilizer rates were
calculated based on a target yield (6.0Mg ha−1 for winter wheat,
4.0 Mg ha−1 for spring wheat), available soil nitrate-N, N mineraliza-
tion from the previous year’s leguminous residues where present
(20 kg ha−1 prior to 2013 and 30 kg ha−1 since 2013 if harvested for
grain; 30 kg ha−1 prior to 2013, 60 kg ha−1 from 2013 to 2015, and
45 kg ha−1 since 2016 if used for hay or manure), and N mineralization
from soil organic matter over winter (25 kg ha−1) based on previous
soil lab test results. Urea fertilizer was applied by subsurface banding at
sowing.
2.2. Soil sampling
Two soil cores per plot per sampling date were extracted 21 April
2017, prior to sowing spring crops or implementing fallow practices,
and 6 July 2017, while crops were actively growing in the field.
Sampling immediately prior to planting provided a snapshot of the
nematode community present for plant colonization, while sampling
during the growing season indicated succession within the community
after plant colonization. One core was used to determine gravimetric
and volumetric soil moisture to standardize nematode counts on a dry
soil weight basis and the second core was used for nematode extraction
and faunal analysis. Each sample was put in a polypropylene-lined tin-
tie soil bag (i.e., ‘coffee’ bag) and placed inside a cooler immediately
after sampling for transport. Samples were refrigerated at 4 °C until
processing, typically within two weeks of extraction.
2.3. Soil nematode analysis
Soil extractions of no less than 25 g of fresh soil were performed
using the Baermann funnel technique (Flegg and Hooper, 1970). Ex-
tractions ran for 72 h, after which water suspension samples of at least
15mL were collected. Nematodes were counted and identified on a
nematode counting slide (Chalex Corp.) using a Motic® AE2000 in-
verted microscope with phase contrast. Nematode density was adjusted
to total individuals per 100 g on a dry soil basis. Nematodes were as-
signed to a trophic group, a cp value, and a functional guild (Bongers,
1990; Bongers et al., 1995; Freckman and Ettema, 1985; Freckman and
Ettema, 1993). Community structure was assessed using trophic group
and cp value information and the following ecological indices: Maturity
Index, Σ Maturity Index, Plant Parasitic Index, Basal Index, Structure
Index, and Enrichment Index (Bongers, 1990; Bongers and Bongers,
1998; Ferris et al., 2001; Freckman and Ettema, 1993; Yeates et al.,
1993). Composite, enrichment, structure, herbivore, fungivore, bac-
terivore, omnivore, and carnivore metabolic footprints were calculated
for components of the nematode community as described by Ferris
(2010). Calculations of C respiration footprints were facilitated using
the Nematode INdicator Joint Analysis (NINJA) 2.0 (http://
ninjanemaplex.ucdavis.edu/main/) R Shiny application developed by
Sieriebriennikov et al. (2014).
2.4. Statistical analysis
Data were subject to analysis of variance (ANOVA) for a randomized
complete block design using the lmer function in the lme4 mixed-effects
model package in R version 3.3.2 (Bates et al., 2015; R Core Team,
2013), where cropping system was a fixed effect and block was a
random effect. Linear contrasts among cropping systems means were
A. Burkhardt et al. Applied Soil Ecology 136 (2019) 93–100
94
conducted using the emmeans package (Lenth, 2017) between the CRP
conversion and the wheat-pulse grain rotations to better assess the
perennial effect from CRP, between the tilled fallow (wheat-tilled
fallow) and no-till fallow (wheat-chemical fallow) systems to assess the
impact of tillage, and between the wheat-chemical fallow and con-
tinuous wheat to assess the impact of fallow versus annual cropping.
Where the assumptions of normality and homoscedasticity were not
met, data were transformed using ln(x+ 1) prior to analysis. Back-
transformed data means are reported. Differences among treatment
means were assessed using a protected LSD post-hoc at α < 0.05.
Non-metric multidimensional scaling (NMDS) was used to assess the
data and provide a framework for analysis of the significance and effect
sizes of candidate explanatory variables using the labdsv package in R
(Roberts, 2016). Briefly, a Bray-Curtis dissimilarity matrix was calcu-
lated from ln(x+1) transformed taxon abundance data. To generate
the NMDS results, the minimum stress result was calculated from 100
random starts for both two- and three-dimensional solutions. The
lowest dimensionality results with a stress of less than 20 were selected
for further analysis.
Explanatory variables of interest were fitted to the ordination with a
generalized additive model (GAM) using the ordination coordinates as
explanatory variables, and appropriate error structures for individual
variables (Gaussian for environmental variables, negative binomial for
species abundances). Goodness-of-fit was assessed with deviance ex-
plained (D2=1− (residual deviance/null deviance)) and considered
significant for D2 values ≥0.70.
3. Results
Forty genera of nematodes were identified across the cropping
systems in 2017 (Supplementary Tables 1 and 2). Nematode taxa counts
were standardized by relative abundance of individuals per 100 g dry
Fig. 1. Precipitation (bars) and maximum (dotted line) and minimum (solid line) daily soil temperature at 5 cm below bare ground at the Arthur H. Post Research
Farm for 2017. Dashed lines indicate sampling dates, 21 April and 6 July. Total precipitation between sampling dates was 156mm.
Table 1
Cropping sequences and cumulative applied nitrogen fertilizer for all systems.
Cropping system Wh-Tilled
Fallow
Wh-Chemical
Fallow
Continuous Wh Wh-Pulse
Gr
Wh-Pulse For Wh-Pulse Man Org. Wh-
Pulse
CRP conversion
Tillage tilled no-till
2-year sequence 2003–2008 fallow-w wh fallow-w wh spr wh-w wh w pea (gr)-
w wh
w pea (for)-w
wh
w pea (for)-spr
wh
w pea (gr)-
w wh
alfalfa-grass
mixture
4-year sequence 2009 fallow fallow spr wh spr pea (gr) spr pea (for) spr pea (man)† spr pea (gr)
2010 spr wh spr wh spr wh spr wh spr wh spr wh spr wh
2011 fallow fallow w wheat spr pea (gr) spr pea (for) spr pea (man) spr pea (gr)
2012 w wh w wh w wh w wh w wh w wh w wh
2013 fallow fallow spr wh spr pea (gr) spr pea (for) spr pea (man) spr pea
(man)
spr pea (gr)
2014 spr wh spr wh spr wh spr wh spr wh spr wh spr wh spr wh
2015 fallow fallow w wh w pea (gr) w pea (for) w pea (man) w pea
(man)
w pea (gr)
2016 w wh w wh w wh w wh w wh w wh w wh w wh
2017 fallow fallow spr wh spr lentil
(gr)
3 sp CCM
(forage)‡
3 sp CCM
(manure)
spr lentil
(gr)
spr lentil (gr)
Cumulative applied N
fertilizer
kg ha−1 1146 1185 2300 1075 983 811 0 214
§w=Winter, spr= Spring, wh=wheat, for= forage, gr= grain, man=manure, sp= species, CCM= cover crop mix.
† Where a pulse manure was grown, termination was achieved through herbicide application at first bloom, except in the case of the organic system, where
termination was achieved at first bloom with tillage.
‡ Cover crop mix comprised the following: fababean, proso millet, and tillage radish.
A. Burkhardt et al. Applied Soil Ecology 136 (2019) 93–100
95
soil.
3.1. Evaluation of nematode community dimensionality
During exploratory analysis with NMDS, three dimensions were
found to reduce stress below 20 (stress= 18.6). Distances among points
in the ordination were highly correlated (r=0.89) with the original
data. Within the first two dimensions, total population and fungivore
footprint explained significant proportions of the dissimilarity, with
D2=0.71 and 0.70, respectively (Fig. 2, left panel). From this we can
assert that where total population is greater there is a high likelihood of
a higher fungivore footprint. Within the first and third dimensions,
species richness and bacterivore footprint had significant D2, both at
0.75 (Fig. 2, right panel). Within these two dimensions, we can assert
that where species richness is greater so is the bacterivore footprint.
The second versus third dimensions had no D2 greater than 0.70. NMDS
failed to show any significant separation or clustering of cropping
system, but it did show clustering of sampling date when viewed from
this perspective (Fig. 3). This clustering of sampling dates likely re-
presents the difference in soil environment from pre-plant to in-season
sampling. Gravimetric soil moisture declined by an average of 5%
across all cropping systems and soil temperature increased roughly
10 °C at 5 cm under bare ground between sampling dates (Fig. 1).
NMDS confirmed associations among nematode communities.
3.2. Cropping systems effects
Prior to planting, Basal Index, a measure of the abundance of stress
tolerant nematodes, was higher under wheat-chemical fallow and
wheat-pulse hay (72 and 69, respectively) than under continuous
wheat, wheat-pulse manure, organic wheat-pulse grain, and CRP con-
version (47, 48, 46, and 47, respectively, Table 2), indicating increased
stress to the nematode community under wheat-chemical fallow and
wheat-pulse hay. Conversely, Enrichment Index was higher under
continuous wheat, wheat-pulse manure, organic wheat-pulse grain, and
CRP conversion (38, 42, 43, and 37, respectively) than the wheat-
chemical fallow treatment (19, Table 2), indicating low resource
availability for nematodes under wheat-chemical fallow. Both ∑ Ma-
turity Index, the whole nematode community maturity, and Plant
Parasitic Index, were higher under CRP conversion (2.6 and 3.0, re-
spectively, Table 2) than no-till and organic wheat-pulse grain (2.3 and
2.6 under no-till and 2.2 and 2.5 under organic) and wheat-pulse
manure (2.3 and 2.6). These higher indices indicate both an increase in
higher cp, stress susceptible nematodes, and a higher abundance of high
cp value herbivores, particularly Helicotylenchus, Pratylenchus, and
Fig. 2. Non-metric dimensional scaling surface plots. The panel on the left shows the total population (black) and fungivore footprint (grey) on the x and y axes; while
the panel on the right shows the bacterivore footprint (black) and species richness (grey) on the x and z axes. These four response variables explained the largest
proportion of the dissimilarity in the data. However, both metabolic footprints skewed largely to the right, whereas total population and species richness had greater
capture of the data’s dissimilarity.
Fig. 3. Three-dimensional model of the NMDS, showing grouping of the data by
sampling date (grey= pre-plant, black= in-season). Axes indicate the opti-
mized dissimilarity of the data. Overlap was observed, but in general sampling
date did cluster together. We hypothesize that sampling date clustered together
due to environmental changes from April to July. Gravimetric soil moisture
decreased an average of 5% between sampling dates while air temperature
increased roughly 15 °C in that same time.
A. Burkhardt et al. Applied Soil Ecology 136 (2019) 93–100
96
Tylenchorhynchus.
3.3. Tillage effects
Tillage negatively impacted total abundance of nematode. Total
nematodes, total free-living nematodes, and total cp 2–5 nematodes
were all higher under chemical fallow compared to tilled fallow prior to
planting (Tables 3 and 4), meaning reduced populations in the spring
were directly linked to tillage. During the growing season, a higher
proportion of fungivores and the fungivore footprint occurred under
tilled fallow (Tables 2 and 4), indicating higher fungal hyphae density
or higher abundance of fungi susceptible to nematode predation under
tillage. Cp 3 herbivores were higher under chemical fallow (Table 3).
3.4. Fallow effects
Fallow had little effect on the nematode community structure but
did impact population totals. Total free-living and total cp 2–5 nema-
todes were higher prior to planting under wheat-chemical fallow than
continuous wheat (Tables 3 and 4). During the growing season, no
significant effects were observed.
3.5. Effects of perennation
Perennation had both positive and negative effects on community
structure. When the wheat-pulse grain rotation was compared to the
CRP conversion, we observed higher ∑ Maturity Index, Plant Parasitic
Index, and cp 3 herbivores under CRP conversion prior to planting,
indicating more stress susceptible genera and more PPNs of economic
importance were present under CRP conversion. Cp 2 herbivores were
higher under wheat-pulse grain prior to planting. During the growing
season, cp 4 nematodes and proportion of omnivores were higher under
CRP conversion (Tables 3 and 4). The ∑Maturity Index accounts for the
cp value of the whole community, while the Plant Parasitic Index only
accounts for the cp value of the herbivorous portion. The increase in
these two indices was largely due to higher abundance of cp 3 and 5
PPNs and cp 4 omnivores under CRP conversion.
4. Discussion
Tillage, cropping system, sampling date, and previous perennation
are the key factors influencing nematode communities in this study.
Tillage deleteriously affects the nematode community structure by
creating physical disturbance that reduces the abundance of stress
susceptible nematodes. We observed our largest total population var-
iations in the spring and by summer, those variations were gone, and
the differences observed were within the structure of the population.
The population declines were likely associated with a decrease in soil
moisture and increases in soil temperature, as noted by both Bakonyi
et al. (2007) and Thompson et al. (2018). Fewer free-living nematodes
and cp 2–5 nematodes were observed under a continuous wheat system
versus wheat-chemical fallow. This is counter to a study by Govaerts
et al. (2007) in corn-wheat systems in Mexico, where nematode popu-
lations were higher under continuous wheat.
The nematode communities were different under tillage versus no-
till. The tillage effects we measured—a decreased population prior to
tillage, coupled with an increase in fungivores after tillage—corrobo-
rate those of Ito et al. (2015a,b), where total nematode population
under rice-soybean systems in Japan were detrimentally affected by
tillage even though total fungivores increased. However, our results
Table 2
Ecological indices and metabolic footprints of the nematode community from different crop rotations at two sampling dates (standard error).
Treatment Sampling Date Ecological Indices Metabolic Footprints
Basal Index Enrichment Index ∑ Maturity Index Plant Parasitic Index Herbivore Fungivore
μg C kg−1
Cropping system
Wheat-Tilled Fallow 21-Apr-17 62(5) ab 28(3) abc 2.3(0.0) bc 2.8(0.0) abcd 41(9) 29(7)
Wheat-Chemical Fallow 21-Apr-17 72(6) a 19(4) c 2.3(0.1) bc 2.7(0.1) abcd 94(15) 36(5)
Continuous Wheat 21-Apr-17 47(4) b 38(3) ab 2.5(0.0) ab 2.9(0.1) abc 69(22) 30(4)
Wheat-Pulse Grain 21-Apr-17 63(5) ab 23(3) bc 2.3(0.1) bc 2.6(0.1) bcd 65(15) 21(7)
Wheat-Pulse Forage 21-Apr-17 69(3) a 22(2) bc 2.4(0.1) abc 2.9(0.1) ab 61(17) 30(9)
Wheat-Pulse Manure 21-Apr-17 48(4) b 42(4) a 2.3(0.1) bc 2.6(0.1) cd 76(20) 28(7)
Org. Wheat-Pulse 21-Apr-17 46(9) b 43(12) a 2.2(0.1) c 2.5(0.2) d 120(56) 41(11)
CRP conversion 21-Apr-17 47(4) b 37(3) ab 2.6(0.1) a 3.0(0.0) a 112(18) 31(5)
Wheat-Tilled Fallow 06-Jul-17 42(5) 38(3) 2.3(0.1) 2.5(0.1) 208(73) 56(67)‡
Wheat-Chemical Fallow 06-Jul-17 42(8) 37(7) 2.6(0.1) 2.8(0.1) 51(10) 10(3)
Continuous Wheat† 06-Jul-17 39(5) 34(2) 2.4(0.1) 2.4(0.1) 34(54) 21(6)
Wheat-Pulse Grain 06-Jul-17 47(4) 31(4) 2.3(0.0) 2.6(0.1) 31(11) 12(4)
Wheat-Pulse Forage 06-Jul-17 44(7) 48(7) 2.2(0.1) 2.6(0.1) 134(30) 44(9)
Wheat-Pulse Manure 06-Jul-17 45(4) 49(6) 2.2(0.1) 2.7(0.1) 56(15) 28(11)
Org. Wheat-Pulse 06-Jul-17 43(4) 35(4) 2.3(0.0) 2.3(0.0) 66(11) 37(4)
CRP conversion 06-Jul-17 37(5) 31(5) 2.5(0.1) 2.5(0.1) 80(28) 18(5)
ANOVA df p values
Cropping system 21-Apr-17 7 0.03* 0.04* 0.04* 0.03* 0.62 0.91
06-Jul-17 7 0.97 0.22 0.28 0.11 0.41 0.21
1 df contrast
Tilled vs chemical fallow 21-Apr-17 1 0.32 0.26 0.90 0.84 0.24 0.61
06-Jul-17 1 0.99 0.92 0.14 0.06 0.07 0.02*
Fallow vs annual 21-Apr-17 1 0.09 0.14 0.36 0.99 0.99 0.52
06-Jul-17 1 0.84 0.48 0.13 0.42 0.20 0.94
CRP vs. Wheat-Pulse grain 21-Apr-17 1 0.09 0.11 0.01* 0.02* 0.29 0.48
06-Jul-17 1 0.35 0.98 0.19 0.78 0.56 0.56
§Numbers followed by the same letter are not significantly different at P < 0.05 based on one-way ANOVA followed by an LSD test.
* Significant at p < 0.05.
† Based on three replicates.
‡ Back-transformed from ln(x+ 1).
A. Burkhardt et al. Applied Soil Ecology 136 (2019) 93–100
97
contradict those from Griffiths et al. (2012) in the United Kingdom for a
continuous barley system and those from Sharma-Poudyal et al. (2017)
for dryland wheat cropping systems in the Pacific Northwest, where
abundance of fungivores increased under zero and minimum tillage
systems compared to moldboard or chisel plow. Griffiths et al. (2012)
correlated their findings in the nematode community with their de-
tection of an increased proportion of fungi in the microbial community
under no-till and minimum till practices.
In our study, tillage negatively affected cp 3 herbivores as a per-
centage of total herbivores during the growing season, but total her-
bivore abundance remained three-fold higher under tilled fallow. Thus,
tillage served to simplify the nematode community but did not reduce
the total population. In fact, our research suggests that tillage en-
couraged a large flush of opportunistic nematodes, as evidenced by the
higher Basal Index during the spring and the higher proportion of op-
portunistic fungivores during the summer under tilled fallow.
The effects of annual cropping were less pronounced. Continuous
wheat, wheat-pulse manure, organic wheat-pulse, and CRP conversion
had a higher pre-plant Enrichment Index and lower Basal Index than
wheat-chemical fallow, but not wheat-tilled fallow. The low Basal Index
under CRP conversion, organic wheat-pulse, wheat-pulse manure, and
continuous wheat is likely due to more crop residue being returned to
the soil, in contrast to both wheat-chemical fallow and wheat-pulse
forage. The high Enrichment Index may be for similar reasons. Few
studies have associated the effects of fallow on nematode populations,
and those that have made associations have focused largely on the PPN
population (Stirling et al., 2001; Thompson et al., 2012). Our study is
the first to make associations about nematode community structure
under fallow versus annually cropped systems.
A legacy of perennation within one cropping system was associated
with a more stable and mature nematode community in the current
study. CRP has been shown to have beneficial impacts to soil microbial
communities in the Southern Great Plains (Li et al., 2018), providing
crucial pollinator and wildlife habitat (Grovenburg et al., 2011; Otto
et al., 2018), and playing an important role in soil C storage (Engel et al.
2017; O’Connell et al., 2016). In our study, the CRP conversion system
had higher pre-plant Σ Maturity Index, Plant Parasitic Index, and per-
centage cp 3 herbivores, as well as greater proportions of omnivores
and cp 4 nematodes in the growing season, indicating a nematode
community comprised of infrequent, predominantly omnivorous, and
higher cp value nematodes. Higher abundance of these cp 3–5 nema-
todes under CRP conversion suggests a more balanced soil food web
than the other cropping systems. The proportion of cp 4 nematodes
under CRP conversion was nearly triple that of the wheat-pulse grain
rotation, and the proportion of omnivores was similarly high. Under
CRP conversion, the higher Σ Maturity Index was driven by the higher
proportion of omnivores and the Plant Parasitic Index was driven by the
higher percentage of cp 3 herbivores. Unpublished data from the study
comparing the wheat-pulse grain system to the CRP system under
conversion indicate that following conversion, soil moisture, yield, and
net returns were less, while soil N supply was higher (P. Miller, personal
communication). Reduced wheat yield in the system has been attrib-
uted to the high soil N due to ‘haying off’, however the higher cp 3
herbivores under CRP conversion were dominated by genera important
to crop production including Pratylenchus, Helicotylenchus, and Ty-
lenchorhynchus.
Both high soil N and high abundance of herbivores in the system
may have contributed to a negative impact to crop production. The
Table 3
Cp value compositions for cropping systems at two sampling dates (standard error).
Treatment Sampling Date Total cp 2–5 Free-living cp 4 Herbivores
cp 2 cp 3 cp 5
Cropping system %
Wheat-Tilled Fallow 21-Apr-17 1275 (330) 3 (2) 22 (4.3) ab 76 (4.6) abcd 0 (0)
Wheat-Chemical Fallow 21-Apr-17 3196 (632) 5 (1) 18 (6.2) abc 74 (6.2) abcd 0 (0)
Continuous Wheat 21-Apr-17 882 (86) 11 (3) 12 (8.2) bc 86 (8.2) abc 0 (0)
Wheat-Pulse Grain 21-Apr-17 1461 (619) 7 (2) 29 (7) ab 64 (6.9) bcd 0 (0)
Wheat-Pulse Forage 21-Apr-17 1430 (360) 4 (1) 6 (8.2) cd 91 (8.2) ab 0 (0)
Wheat-Pulse Manure 21-Apr-17 1021 (242) 5 (1) 32 (9.6) ab 59 (9.5) cd 0 (1)
Org. Wheat-Pulse 21-Apr-17 1164 (253) 7 (2) 45 (17.6) a 46 (17.6) d 0 (0)
CRP conversion 21-Apr-17 1055 (187) 8 (2) 2 (0.6) d 96 (1.1) a 1 (1)
Wheat-Tilled Fallow 06-Jul-17 1816 (861)‡ 7 (2) 54 (7.9) 43 (8.2) 3 (1)
Wheat-Chemical Fallow 06-Jul-17 509 (205) 12 (3) 19 (9.2) 80 (9.4) 1 (1)
Continuous Wheat† 06-Jul-17 758 (213) 13 (3) 59 (12.5) 41 (12.5) 0 (0)
Wheat-Pulse Grain 06-Jul-17 635 (166) 7 (3) 43 (10.6) 57 (10.6) 0 (0)
Wheat-Pulse Forage 06-Jul-17 1383 (678) 4 (1) 40 (8.7) 59 (8.4) 1 (1)
Wheat-Pulse Manure 06-Jul-17 825 (327) 2 (2) 29 (9.5) 71 (9.6) 0 (1)
Org. Wheat-Pulse 06-Jul-17 1033 (157) 14 (3) 71 (3.3) 29 (3.3) 0 (0)
CRP conversion 06-Jul-17 1053 (230) 23 (7) 49 (7.1) 51 (7.1) 0 (0)
ANOVA df p values
Cropping system 21-Apr-17 7 0.06 0.43 < 0.01** 0.04* 0.45
06-Jul-17 7 0.62 0.22 0.14 0.17 0.65
1 df contrast
Tilled vs chemical fallow 21-Apr-17 1 0.01* 0.67 0.77 0.84 N/A
06-Jul-17 1 0.07 0.50 0.05 0.05* 0.33
Fallow vs annual 21-Apr-17 1 0.02* 0.21 0.58 1.00 0.88
06-Jul-17 1 0.79 0.56 0.63 0.75 0.10
CRP vs. Wheat-Pulse grain 21-Apr-17 1 0.56 0.87 < 0.001*** 0.04* 0.06
06-Jul-17 1 0.46 0.05* 0.76 0.75 0.83
§Numbers followed by the same letter are not significantly different at P < 0.05 based on one-way ANOVA followed by an LSD test.
* Significant at p < 0.05.
** Significant at p < 0.01.
*** Significant at p < 0.001.
† Based on three replicates.
‡ Back-transformed from ln(x+ 1).
A. Burkhardt et al. Applied Soil Ecology 136 (2019) 93–100
98
differences in Σ Maturity Index and Plant Parasitic Index were not
observed during the growing season, and we hypothesize that de-
creasing water availability in the soil begins to have a dominant effect
on the nematode community as the growing season progresses. The
higher abundance of omnivores during the growing season may also be
influencing herbivore abundance through predation.
Berkelmans et al. (2003) suggested the use of Basal Index and
Structure Index as soil health indicators, where high Basal Index would
indicate poor soil ecosystem health and high Structure Index would
indicate a healthy, steady soil ecosystem. While no differences in
Structure Index were observed among cropping systems, CRP conver-
sion had the lowest Basal Index, suggesting that more stress susceptible
nematode taxa were present in the community as supported by the Σ
Maturity Index and proportion of omnivores in the nematode commu-
nity. This low Basal Index indicate there could be an advantage for the
inclusion of a perennial phase to overall soil health.
Our results suggest a benefit from decreasing soil disturbance and
including a perennial crop phase in semi-arid wheat production systems
on fostering a more balanced and interconnected soil nematode com-
munity. Similarly, soil organic C and soil total N also were favored by
reductions in tillage and perennation in the same field experiment
(Engel et al., 2017), with both being elevated in the top 10 cm under
CRP compared to all cropping systems. We speculate that where soil
organic C has been significantly increased, there is a benefit to soil
nematodes.
Cumulative fertilizer application and associated changes in soil pH
likely impacted nematodes in our study. Cumulative N fertilizer appli-
cation was markedly reduced in the CRP conversion compared to all
conventionally managed systems (e.g., 214 kg ha−1 for the CRP
conversion compared to 2300 kg ha−1 for continuous wheat).
Unpublished data from this study indicated greater soil pH for the CRP
conversion system compared with the continuous wheat system.
However, without additional soil pH and N data, our associations to soil
chemistry are only speculative. Any future work will require detailed
soil chemical analysis in tandem with a soil nematode community
analysis to understand how soil chemistry impacts the nematode
community.
5. Conclusions
Our study highlights the interaction between cropping system and
the soil nematode community. A legacy effect from perennation to
multiple components of the nematode community was observed four
years after conversion from a perennial to annual cropping system.
Further work is necessary to add to our knowledge of the nematode
community in such a perennial system and how converting it to annual
cropping systems affects the nematode community. The effect of tillage
was observed in decreased total population prior to planting in the
spring.
Fostering a more diverse nematode community is a means to
achieving sustainable production, but the possibility of further in-
corporating management practices into PPN management by better
understanding how PPNs are affected by crop rotation and management
warrants further research. This is the first published work comparing
CRP versus annual cropping systems to nematode community structure.
Our sampling of the study was done four years after the conversion
from CRP, and effects from perennation were still evident. What these
effects were in the first year and how long the effects will linger is not
Table 4
Population totals and guild compositions for different crop rotations at two sampling dates (standard error).
Treatment Sampling Date Total Total free-living Total community
Fungivores Omnivores
%
Cropping system
Wheat-Tilled Fallow 21-Apr-17 1712 (393) 1314 (346) 19 (4) 2 (1.0)
Wheat-Chemical Fallow 21-Apr-17 4201 (606) 3215 (634) 11 (2) 2 (0.5)
Continuous Wheat 21-Apr-17 1665 (216) 904 (92) 25 (4) 8 (2.6)
Wheat-Pulse Grain 21-Apr-17 2058 (684) 1496 (621) 13 (3) 4 (0.8)
Wheat-Pulse Forage 21-Apr-17 2185 (528) 1442 (364) 14 (4) 2 (0.5)
Wheat-Pulse Manure 21-Apr-17 1854 (363) 1112 (265) 24 (4) 3 (0.8)
Org. Wheat-Pulse 21-Apr-17 2139 (421) 1248 (194) 23 (4) 4 (0.4)
CRP conversion 21-Apr-17 2404 (353) 1077 (188) 16 (2) 4 (1.2)
Wheat-Tilled Fallow 06-Jul-17 2600 (1250)‡ 1879 (859)‡ 27 (4) 4 (1.5)
Wheat-Chemical Fallow 06-Jul-17 984 (263) 535 (211) 14 (2) 7 (1.5)
Continuous Wheat† 06-Jul-17 1028 (463) 799 (216) 21 (3) 9 (1.9)
Wheat-Pulse Grain 06-Jul-17 925 (218) 660 (172) 17 (4) 5 (1.5)
Wheat-Pulse Forage 06-Jul-17 2607 (854) 1618 (763) 22 (2) 2 (0.7)
Wheat-Pulse Manure 06-Jul-17 1413 (510) 953 (379) 28 (3) 1 (1.0)
Org. Wheat-Pulse 06-Jul-17 1479 (186) 1038 (160) 31 (5) 10 (2.7)
CRP conversion 06-Jul-17 1504 (402) 1083 (237) 14 (2) 18 (5.6)
ANOVA df p values
Cropping system 21-Apr-17 7 0.09 0.07 0.26 0.51
06-Jul-17 7 0.62 0.65 0.07 0.25
1 df contrast
Tilled vs chemical fallow 21-Apr-17 1 < 0.01** 0.01* 0.23 0.92
06-Jul-17 1 0.15 0.09 0.05* 0.70
Fallow vs annual 21-Apr-17 1 0.05 0.02* 0.36 0.24
06-Jul-17 1 0.70 0.90 0.70 0.75
CRP vs. Wheat-Pulse grain 21-Apr-17 1 0.67 0.55 0.58 0.96
06-Jul-17 1 0.46 0.49 0.66 0.05*
§Numbers followed by the same letter are not significantly different at P < 0.05 based on one-way ANOVA followed by an LSD test.
* Significant at p < 0.05.
** Significant at p < 0.01.
† Based on three replicates.
‡ Back-transformed from ln(x+ 1).
A. Burkhardt et al. Applied Soil Ecology 136 (2019) 93–100
99
known.
Acknowledgements
The authors would like to acknowledge the Montana Wheat and
Barley Committee for their financial support of the project.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.apsoil.2018.12.020.
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