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Renewable Agriculture and
Food Systems
cambridge.org/raf
Research Paper
Cite this article: Pisani Gareau T, Voortman C,
Barbercheck M (2019). Carabid beetles
(Coleoptera: Carabidae) differentially respond
to soil management practices in feed and
forage systems in transition to organic
management. Renewable Agriculture and Food
Systems 1–18. https://doi.org/10.1017/
S1742170519000255
Received: 3 January 2019
Revised: 27 April 2019
Accepted: 30 May 2019
Key words:
Carabid; cover crops; ground beetle; organic
agriculture; organic transition; soil
disturbance; tillage
Author for correspondence:
Tara Pisani Gareau, E-mail: tara.
pisanigareau@bc.edu
© Cambridge University Press 2019
Carabid beetles (Coleoptera: Carabidae)
differentially respond to soil management
practices in feed and forage systems in
transition to organic management
Tara Pisani Gareau1, Christina Voortman2and Mary Barbercheck2
1
Department of Earth and Environmental Sciences, Boston College, Chestnut Hill, MA 02467, USA and
2
Department of Entomology, The Pennsylvania State University, University Park, 501 ASI, PA 16802, USA
Abstract
We conducted a 3-yr cropping systems experiment in central Pennsylvania, USA, to deter-
mine the effects of initial cover crop species, tillage and resulting environmental variables
on the activity–density (A–D), species richness, community composition and guild compos-
ition of carabid beetles (Carabidae: Coleoptera) during the transition from conventional to
organic production. We compared four systems in a factorial combination of a mixed peren-
nial sod (timothy, Phleum pratense L.) and legumes (red clover, Trifolium pratense L.) or
annual cereal grain (cereal rye, Secale cereale L.) followed by a legume (hairy vetch, Vicia vil-
losa Roth) as initial cover crops, and soil management using full tillage (moldboard plow) or
reduced tillage (chisel plow) implemented in soybeans followed by maize in the subsequent
year. The experiment was established twice, first in autumn 2003 (S1) and again in autumn
2004 (S2) in an adjacent field, in a randomized complete-block design with four replicates
in each Start. We collected a total of 2181 adult carabid beetles. Approximately 65% of the
carabid beetles collected were from six species. Indicator Species Analysis showed that several
carabid species were indicative of treatment, e.g., Poecilus chalcites was a strong indicator for
treatments with an initial cereal rye cover crop. Eleven environmental variables explained vari-
ation in carabid A–D, richness and the A–D of species categorized by size class and dominant
trophic behavior, respectively, but varied in significance and direction among guilds. Soil
moisture was a significant effect for total carabid A–D in both S1 and S2. Redundancy ana-
lyses revealed some similar and some idiosyncratic responses among informative species for
the cover crop×tillage treatments through the 3-yr rotation. The most consistent factors
that distinguished species assemblages among years and treatments were the number and
intensity of soil disturbances and perennial weed density. The consistent occurrence of soil
disturbance indicators in multivariate analyses suggests that future studies that aim to com-
pare the effects of nominal soil management treatments on carabid beetles and other soil-
associated arthropods should quantify frequency and intensity of disturbance associated
with crop management practices.
Introduction
Organic farming and in-field plant diversification can mitigate negative environmental effects
associated with agricultural intensification by increasing arthropod species and functional
richness and increasing related ecosystem services, such as predation and pollination, to agroe-
cosystems (Norton et al., 2009; Tuck et al., 2014; Lichtenberg et al., 2017). Organic farming on
average increases species richness by 30% and the effect is more pronounced in intensively
managed landscapes (Tuck et al., 2014). In the USA, farmers who want to convert to an
organic farming system are required to undergo a 3-yr transition period in which they forego
the use of non-allowed materials or practices before their land and crops can be certified as
organic (USDA NOP, 2019). Conservation and improvement of soil quality is a stated require-
ment in the USDA organic rule (USDA NOP, 2019) and is a philosophical foundation of
organic production (Heckman, 2006). Transitioning and organic farmers report that weed
and insect pests are among their top challenges and largely rely on cultural practices, conser-
vation biological control and intercropping to manage pests (Zehnder et al., 2007). The object-
ive of this study was to determine how cultural practices for weed management and building
soil quality in the transition to organic production of cereals and forage crops affect the assem-
blage of carabid beetles (Coleoptera: Carabidae), an important group of insects to conserve for
biological control of ground-dwelling arthropod pests and weed seeds (Kromp, 1999;
Lundgren et al., 2006; Hanson et al., 2016).
Carabids are a ubiquitous and abundant group of beetles in terrestrial systems, including
agricultural fields; however, the assemblage of carabid species and trophic groups, and the
functional response vary by habitat type (Larsen et al., 2003;
Aviron et al., 2005; Winqvist et al., 2014). In comparison to
wooded habitat, carabid assemblages associated with agricultural
or herbaceous habitat tend to have a greater proportion of cara-
bids that are herbivorous, smaller-sized and more mobile
(Thiele, 1977; Aviron et al., 2005; Schirmel et al., 2016).
Carabid size is an important determinant of biological control
function, with larger beetles, generally associated with wooded
habitat (Blake et al., 1994), demonstrating lower prey handling
times and higher consumption rates of prey (Rouabah et al.,
2014; Ball et al., 2015). Within agricultural habitats, carabid
assemblages generally have higher species richness and abun-
dance in organic compared to conventional cropping systems
(Pfiffner and Niggli, 1996; Döring and Kromp, 2003; Bengtsson
et al., 2005; Purtauf et al., 2005; Clark et al., 2006; Rondon
et al., 2013). Organic systems favor carabid diversity through
the elimination of synthetic pesticides, which enhances plant
and arthropod food resources for predators and greater plant
diversity and habitat complexity compared with conventional sys-
tems (Andow, 1991; Veselý and Šarapatka, 2008; Jabbour et al.,
2015; Rivers et al., 2017). Rusch et al.(2013) found that an
increase in fallow period and organic farming practices and
reduction in pesticide use over a 24-yr period increased the pro-
portion of large and omnivorous carabid beetles in the agricul-
tural landscape in Sweden.
Organic systems depend on a range of soil disturbance prac-
tices from deep tillage to surface cultivation to control weeds
(Bond and Grundy, 2001) and incorporate animal and green
manures. Soil disturbance practices can result in an overall
decrease in soil faunal biomass and suppression of beneficial
soil organisms, such as arthropod predators (Lundgren et al.,
2006; Tsiafouli et al., 2015). Adult carabid beetles generally forage
on the soil surface, oviposit in and on the soil, and develop
through the egg, larval and pupal stages in the soil. Thus, all
life stages of carabids can be affected by soil disturbances, either
through direct mortality to individuals or change in abiotic and
biotic habitat that can favor or deter particular species (Stinner
and House, 1990; Kromp, 1999; Eyre et al., 2013).
Reducing tillage frequency and intensity (area or volume of dis-
turbed soil) generally has a positive effect on carabids (Lundgren
et al., 2006; Blubaugh and Kaplan, 2015; Jabbour et al., 2015;
Hanson et al., 2016; Rivers et al., 2017). However, some studies
have not found a significant effect of tillage on the overall
abundance of carabid beetles (Cárcamo, 1995; Clark et al., 2006)
and some carabid species are significantly more abundant in con-
ventionally tilled fields (Ferguson and McPherson, 1985; Cárcamo,
1995; Belaoussoff et al., 2003; Menalled et al., 2007). Variable
responses of carabid species to tillage may be due to differences
in beetle size, phenology relative to the depth and timing of soil
disturbances or to environmental factors associated with tillage
regime that affect the microclimate (Hatten et al., 2007) and avail-
ability of food resources (Thorbek and Bilde, 2004; Birkhofer et al.,
2008). Thiele, in his seminal book (1977), surmises that the
presence of carabid species in a particular habitat is largely driven
by abiotic variables of the microclimate.
The crop environment can be a strong predictor of arthropod
community structure (Hance et al., 1990; Booij and Noorlander,
1992; Ellsbury et al., 1998; Puech et al., 2014) as crop species
and crop-specific cultivation practices affect the abiotic and biotic
features of the microenvironment (Kromp, 1999; Holland and
Luff, 2000). For carabid beetles of agricultural fields that are pri-
marily ground-dwelling, crop species and their density may affect
carabid dispersal abilities and protection from predators. Thicker
vegetation can slow the dispersal of ground beetles, while also
providing greater cover from predators, while crops with a more
open canopy can facilitate dispersal, but increase mortality rates
from predators. The crop canopy also affects the microclimate—
light quality, temperature, evapotranspiration, humidity and soil
moisture. The crop environment with its associated flora and
fauna also affects food resources for carabids.
Here, we report the results of a field experiment to assess the
effects of a first-year cover crop and subsequent tillage regimen
on carabid adult beetles during the 3-yr transition period in a
cover crop–soybean–corn rotation initiated with different cover
crop treatments. This research was conducted in the context of
a larger project to assess the effects of cover crop and tillage treat-
ments on soil (Lewis et al., 2011), general arthropod communities
(Jabbour et al., 2015), entomopathogens (Jabbour and
Barbercheck, 2009), weeds (Smith et al., 2009), crop yields and
economic performance (Smith et al., 2011). We hypothesized
that carabid beetle abundance, community composition and
guild (size class and trophic behavior) would vary according to
initial cover crop and tillage treatments due to the level of disturb-
ance and environmental characteristics resulting from practices
associated with each treatment. The guild composition of com-
munities can provide a functional understanding of the effects
of management on trophic interactions in agroecosystems, and
body-size distribution and feeding behavior appear to be valuable
for predicting potential biological control by ground-dwelling
predators (Ribera et al., 2001; Harvey et al., 2008; Schmitz,
2009; Crowder et al., 2010; Koivula, 2011; Rusch et al., 2014;
Hanson et al., 2016). We addressed three main questions: (1)
What are the dominant carabid species in our organic grain system
and are any species indicative of particular cover crop and tillage
treatments? (2) Are carabid beetle guilds (size classes and dominant
trophic behaviors) differentially affected by cover crop and tillage
treatments during the transition to organic production? (3) How
do environmental variables affect carabid beetle activity–density
(A–D), species richness and guild, and carabid community com-
position during the transition to organic production?
Materials and methods
Site
The field experiment was conducted at the Russell E. Larson
Agricultural Research Center (RELARC) near Rock Springs, PA
(40°43′N, 77°55′W, 350 m elevation). The climate is continental
with 975 mm mean annual precipitation and mean monthly tem-
peratures ranging from 3°C (January) to 21.6°C (July). Soils at the
site are shallow, well-drained lithic Hapludalfs formed from lime-
stone residuum (Braker, 1981). The dominant soil type at this
location is a Hagerstown silt loam (fine, mixed, semiactive,
mesic, Typic Hapludalf ). Soil texture in our experimental field
was predominantly clay loam with spatial variability in silt
(range of 39.9–54.7%) and sand (14.0–27.0%) content across the
field. Previously, the site had been conventionally cropped with
a tomato–wheat rotation, with tomato preceding the transition
experiment.
Experimental design and field operations
The 3-yr experiment was managed organically and culminated
with organic certification. During these 3 yr, fields were planted
in cover crops in rotation year 1, soybeans (Glycine max L.) in
2 Tara Pisani Gareau et al.
year 2 and maize (Zea mays L.) in year 3 (Fig. 1). The 2 × 2 fac-
torial design crossed two tillage approaches with two cover crop
treatments in year 1. The experiment was established twice, first
in autumn 2003 and again in autumn 2004 in an adjacent field
(the two experimental Starts are hereafter referred to as ‘S1’and
‘S2’), in a randomized complete-block design with four replicates
in each Start. Each treatment plot measured 24 m × 27 m
(0.065 ha), which is larger than other studies that have found a
significant effect of crop type and management (Lundgren
et al., 2006; Eyre et al., 2012) and large enough to accommodate
trivial movement patterns of carabids (Wallin and Ekbom, 2019).
The site was surrounded by >7 m of the routinely mown grassy
border. Treatments in S2 were off-set by one year relative to S1
(Fig. 1, Supplementary Table S1). S1 and S2 were managed similarly
during the 3-yr rotation; however, in the year before initiating S2,
the entire S2 field was managed organically with a mixed cover
crop of timothy (Phleum pratense L.), oat (Avena sativa L.) and
medium red clover (Trifolium pratense L.). All management prac-
tices followed the USDA National Organic Program guidelines
(Smith et al., 2011; USDA NOP, 2019).
Cover crop and tillage treatments
In consultation with our farmer advisory board, we established
two cover crop treatments common to organic feed grain systems
in the fall preceding rotation year 1, and maintained them over
spring and summer of year 1 (2003–2004 in S1; 2004–2005 in
S2). In one cover crop treatment (RYE), cereal rye (Secale cereale
L. cv. Aroostook) was planted in the fall and managed for grain
and straw production in the summer of year 1. After harvest of
the cereal rye, hairy vetch (Vicia villosa Roth) was planted in
the fall of year 1 and killed in the following spring. In the second
cover crop treatment (TIM), a mixture of timothy (P. pratense L.)
and oat (A. sativa L.) was planted in the fall prior to rotation
year 1. The oat served as a nurse crop to the timothy and died
back over the winter. In the spring of rotation year 1, red clover
(T. pratense L.) and oat were frost seeded into the timothy
grass. The TIM cover crop treatment was managed for sod
formation and forage production (mowed and baled). Due to
differences in ground cover, biomass accumulation and manage-
ment disturbances, each cover crop treatment was assumed to
provide a unique microclimate and habitat that would influence
carabid community structure (Carmona and Landis, 1999;
Jackson et al., 2008; Rivers et al., 2017).
The two tillage treatments were full inversion moldboard
plow-based (FT) and chisel plow- and field cultivator-based, which
hereinafter we refer to as reduced tillage (RT). In the RYE cover crop
treatment, the hairy vetch was killed either by moldboard plow in
FT or by mechanical roller-crimper in RT. The TIM treatment was
first tilled in the spring of rotation year 2, prior to planting soybean.
Through the remainder of the experiment, primary tillage in the FT
treatments was accomplished with a moldboard plow and in the RT
treatments with a chisel plow. Rotary hoe and field cultivator use
was the same in both tillage treatments. In S2, additional cultivation
occurred in maize in RT treatments to improve perennial weed control
(see Supplementary Table S1 for the timing of cultivation practices).
Environmental variables
Disturbance frequency and intensity
While tillage is the most intensive soil disturbance, other distur-
bances such as mowing, rolling the cover crop, tine weeding
and rotary hoeing were also imposed within both tillage treat-
ments, which could cause direct mortality of ground beetles or
cause them to disperse from the plots (Hanson et al., 2016). To
determine the effects of total soil disturbance on carabid beetles,
we estimated the frequency and intensity of soil disturbances for
each of the four experimental treatments. For frequency of dis-
turbance, we counted the number of management practices that
occurred annually between January 1 and pitfall sampling events
within the same year, and accumulated them during each growing
season, starting with the initiation of the experiment in the fall of
2003. For the intensity of disturbance associated with each treat-
ment, we used a USDA Natural Resources Conservation Service
soil disturbance rating (SDR) (NRCS 2002). The SDR, which
ranges from 0 (least disturbance) to 30 (greatest disturbance)
for a field operation, is comprised of the sum of six ratings each
with values from 0 to 5 that estimate the relative severity of dis-
turbance. The six component categories of the SDR include soil
inversion, soil mixing, soil lifting, soil shattering, soil aeration
and soil compaction. The field operation that we employed with
the highest SDR was tillage with a moldboard plow with an
SDR of 29, and one of the lowest was flail mowing with an
SDR of 3. To use the SDR in analyses, we summed the SDR values
associated with each field operation for each treatment that accu-
mulated between January 1 and pitfall sampling events within a
season, and annually during the growing season, starting with
the initiation of the experiment in the fall of 2003. Thus, our dis-
turbance variables for each sample event in each cover crop × till-
age treatment consisted of in-season values for frequency of
disturbance (number of disturbances) and intensity of disturbance
(SDR), each accumulated prior to each sample event, and annual
values that we calculated by accumulating values between January
1 and the last field operation of the season (Supplementary
Table S2). Because all plots were managed the same for each treat-
ment combination, there was no variation in disturbance levels
among plots and thus the treatment values are totals, not averages.
In year 1 of the rotation, the total annual number of distur-
bances and SDR were similar between tillage treatments in S1
but differed more by initial cover crop in S2 (Supplementary
Table S2). By the end of the experiment, the accumulated fre-
quency of disturbance and SDR were generally greater in FT
than in RT treatments, except for the case of FT × TIM in S2,
which had the least number of disturbances and lowest SDR of
all the treatments. Therefore, even though we managed our nom-
inal treatments to achieve less disturbance in RT compared to FT,
quantification of disturbance revealed that this was not always the
case.
Soil analysis
We sampled soils in each Start four times in each rotation year:
May, June–July, August and September–October. On each sam-
pling occasion, three soil samples were collected from random
locations at least 3 m from the edge within each treatment plot.
Each sample was comprised of 15 cores (2.5 cm diameter ×
15.2 cm deep), thoroughly mixed by hand in a bucket, placed
into a plastic bag and stored at 4°C. We used subsamples of soil
from each treatment plot to determine permanganate oxidizable
carbon (hereafter, POC) (Weil et al., 2003; Culman et al., 2012)
and soil moisture, measured as matric potential and gravimetric
soil water content determined by mass loss on drying at 45°C
for 72 h divided by dry soil mass. A portion of each sample was
submitted for analysis to the Agricultural Analytical Services
Laboratory of The Pennsylvania State University for the following
Renewable Agriculture and Food Systems 3
characteristics: phosphorus (P), potassium (K), magnesium (Mg),
calcium (Ca), cation exchange capacity (CEC), soil organic matter
(SOM) by loss-on-ignition (LOI-OM), and trace elements zinc
(Zn), copper (Cu) and sulfur (S). Full soil sampling and process-
ing methods are described in Lewis et al.(2011).
Soil entomopathogens
We used a sentinel insect bioassay method with Galleria mello-
nella as a bait to detect and provide a relative quantification of
entomopathogenic fungi (EPF) (Zimmermann, 1986). The
subsample of soil was homogenized by hand and 250 mL were
placed in a 473-mL plastic container along with 15, last-instar
G. mellonella. Lids were placed on the containers, which were
then stored at 20°C for 10 days, when insect condition was
assessed and categorized as alive, dead from causes other than
fungal infection and potentially infected by EPF. Moribund and
dead larvae exhibiting symptoms or signs of fungal infection
were removed and rinsed briefly in 80% ethanol then in water
and held in sealed humid chambers (59 mL Solo® cups) with a
small piece of moistened Whatman No. 1 filter paper for 7
days. We classified sporulating cadavers as infected with
Metarhizium spp., Beauveria spp. or Isaria spp. based on signs
and symptoms (Goettel and Inglis, 1997). The occurrences of
Beauveria and Isaria were very rare, and therefore we focused
Fig. 1. Management practices in Starts 1 and 2 between 2003 and 2007. The 3-yr rotation is represented between the bold vertical lines.
4 Tara Pisani Gareau et al.
further analyses on Metarhizium (Metschnikoff) Sorokin (Order:
Hypocreales; Family Clavicipitaceae). Full sentinel assay methods
are described in Jabbour and Barbercheck (2009).
Annual and perennial weed density
As described in Smith et al.(2009,2011), we assessed the effects
of the initial cover crop and tillage treatments on the density of
weeds that emerged from the existing seed bank each season.
Weed densities were assessed by counting all weeds present in
five, 0.25 m
2
quadrats randomly placed in each treatment plot,
at least 3 m from the edge of the plot. Weed density measure-
ments were made before each disturbance (e.g., mowing, cultiva-
tion) if multiple disturbances occurred within a growing season.
Weed density data were summed to determine the cumulative
weed density in each plot for each growing season. For analyses
and presentation, the data were separated into annual and peren-
nial weed species.
Carabidae sampling
We used a pitfall sampling method to assess the A–Dof
ground-dwelling Carabidae beetles (Morrill et al., 1990). Three
traps, each with a 114 mm mouth diameter, were randomly
placed in each plot, at least 3 m from plot edges, and buried
129 mm deep so that the tops of the traps were flush with the
soil surface. The traps were opened for 72 h, and then the con-
tents were collected, traps were removed from the field and con-
tents processed in the laboratory. Pitfall traps were collected in
2004 (June 21, August 6 and October 7), 2005 (June 20, July 28
and October 21), 2006 (July 3, August 21 and November 2) and
2007 (July 2 and November 1) (Supplementary Table S1). S1
was sampled from 2004 to 2006, and the S2 was sampled from
2005 to 2007.
We identified adult carabid beetles using taxonomic keys
(Downie and Arnett, 1996; Ciegler and Morse, 2000; Bousquet,
2010) and voucher specimens from other studies at the
RELARC (Leslie et al., 2010). Identifications were confirmed by
Mr Robert Davidson (Carnegie Museum of Natural History,
Pittsburgh, PA, USA) and nomenclature was derived from
Bousquet (2012). We obtained information regarding the ecology,
dominant trophic behavior, phenology and size of the adults of
each carabid species from various literature sources (Larochelle
and Larivière, 2003; Lundgren, 2009; Bousquet, 2010; Bohan
et al., 2011; Eyre et al., 2012; Dearborn et al., 2014) and an on-line
source (Homburg et al., 2014). We classified adult carabids into
two types of ecological guilds: size classes and trophic groups
(predominant feeding behavior). Size classes were assigned as:
small, less than 5 mm; medium, between 5 and 10 mm; and
large, greater than 10 mm in length (Eyre et al., 2012). We char-
acterized carabid trophic groups as carnivorous, feeding primarily
on animal tissues; omnivorous, feeding on both animal and plant
tissues; and granivorous, feeding primarily on plant materials,
including seeds (Lundgren, 2009). We archived voucher speci-
mens at the Carnegie Museum of Natural History and at the
Frost Entomological Museum at the Pennsylvania State
University.
Statistical analyses
The A–D of adult carabid beetles was summed over the three pit-
fall traps per treatment plot for each sample date and represented
the number of individuals captured per plot per 72 h for each
species. To determine the dominant carabid species and whether
any species were indicative of particular cover crop and tillage
treatments, we calculated indicator values (IVs) for carabid beetle
species among treatments using Indicator Species Analysis, a non-
parametric procedure in the PC-ORD v.5 (Dufrêne and Legendre,
1997; De Cáceres and Legendre, 2009). The IV is the product of
the relative abundance (in this case A–D) and relative frequency
of the insect species in the sampled habitat, and ranges between
0 (no occurrence) and 100 (exclusive occurrence in the habitat).
We used a Monte Carlo randomization procedure to determine
the statistical significance (P< 0.10) for the maximum IV, repre-
senting the probability of obtaining the same or higher IV with
subsequent tests given the species distribution, among treatments.
Associations with a specific tillage by cover crop treatment are
reported based on the highest IV for each species (De Cáceres
and Legendre, 2009).
To determine the effect of cover crop and tillage treatments on
carabid beetle functional guilds, as represented by size class and
dominant feeding behavior, we used univariate and multivariate
statistical procedures. We used repeated measures split-plot
mixed models with PROC MIXED (SAS Institute Inc., 2004)to
test whether the A–D of carabid beetle guilds differed between
years in the rotation, and cover crop and tillage treatments.
Tillage treatment (FT or RT) was considered the main plot treat-
ment and initial cover crop (RYE or TIM) the subplot treatment.
The A–D of carabids was transformed with the formula log
10
(x+1)
to achieve normality and equal variances. We accounted for
repeated sampling at the same site throughout the experiment
by including an auto-regressive covariance matrix in the model
(Stokes et al., 2000). Data from each experimental Start were
analyzed separately. Block was coded as a random variable.
To identify environmental variables with a significant effect on
the variation in total A–D, species richness and A–Dineach
guild, we used forward selection multiple linear regression with
JMP Pro®13.0 (SAS Institute Inc., 2019). The pool of explanatory
environmental variables included annual and perennial weed
densities, weed diversity, soil properties (POC, LOI-OM, K, Mg,
P, Cu, Zn, Ca, S, CEC, EC, pH and soil moisture), proportion
of sentinel G. mellonella larvae infected by Metarhizium and
number and intensity (SDR) of disturbances within the year
prior to pitfall sampling. Untransformed data are presented in
tables and figures.
To explore the relationship between carabid beetle species and
environmental variables, we conducted a partial redundancy ana-
lysis (RDA) constrained by the four cover crop × tillage treatments
with ‘CANOCO’for Windows version 5.0 (Šmilauer and Lepš,
2014). The mean A–D of carabid beetle species per plot (n=3
traps per plot) occurring in greater than 20% of samples were
included in the RDA. RDA results are displayed graphically
with bi-plot scaling focused on standardized and centered inter-
taxon distances, where carabid species with a fit to the model of
at least 20% are represented as solid line vectors. Significant envir-
onmental variables were projected as dashed line vectors onto the
bi-plots as passive supplementary response variables (Ter Braak
and Šmilauer, 2012).
Results
Treatment effects on carabid species
We collected a total of 2181 adult ground beetles, comprising
1.4% of all arthropods, from 26 genera and at least 58 species
Renewable Agriculture and Food Systems 5
(Supplementary Table S3). We collected 42.6% more carabids in
S1 (1281) than in S2 (899) (Table 1). There were 34 and 55%
more carabids in full tillage plots in S1 and S2, respectively.
Species richness showed less variation between the starts (46 in
S1 and 47 in S2) and was the same between tillage treatments
in both starts. Three to six more species were found in the RYE
plots under full tillage in S1. Approximately 65% of the carabid
beetles were from six species, in order of greatest to least A–D:
Poecilus chalcites (Say), Bembidion quadrimaculatum (Say),
Harpalus pensylvanicus (DeGeer), Cicindela punctulata
(Olivier), Poecilus lucublandus (Say) and Bembidion rapidum
(LeConte). The large carnivore, P. chalcites, the small omnivore,
B. quadrimaculatum, and large granivore, H. pensylvanicus,
comprised 18, 17 and 12%, respectively, of the ground beetles col-
lected. Fifteen species were extremely rare in samples, where only
one individual was collected over the course of the 4-yr study. Five
species had a total of two specimens collected.
Several carabid species were significant indicators for specific
tillage × cover crop treatments, and these results varied between
S1 and S2 (Fig. 2). In S1, Agonum muelleri (Herbst) was an indi-
cator species for FT × RYE (IV = 29, P= 0.0426) (Table 2). The
A–DofA. muelleri was greatest in year 1 and then was not active
in these plots again until year 3. B. quadrimaculatum was an indi-
cator species for RT × RYE (IV = 36, P= 0.0558). The A–DofB.
quadrimaculatum increased over the 3-yr period in these treat-
ment plots. Stenolophus comma (Fabricius) was an indicator spe-
cies for FT × RYE (IV = 29, P= 0.0628). We did not detect S.
comma in any of the treatment plots until year 3, when it was pre-
dominantly active in FT × RYE. In S2, Harpalus herbivagus (Say)
was an indicator species for RT × TIM; while the overall A–Dof
this species was relatively low, in 2006 and 2007 it was almost
exclusively found in RT × TIM (Table 3,Fig. 2). The maximum
IV for P. chalcites was significantly higher in the RT × RYE treat-
ment (P= 0.008). However, for both starts, the IV for RYE treat-
ments ranged from 26 to 40 indicating that P. chalcites is common
and abundant throughout the rotation in the RYE treatment plots
(Fig. 2). Finally, P. lucublandus was an indicator species for the
RT × RYE treatment (IV = 35, P= 0.0992).
Treatment effects on carabid guilds
Carabid size classes
The A–D of carabids (total of three pitfall traps per plot per 72 h)
categorized by size class of carabids was affected by several experi-
mental factors. Year in the rotation was the most frequent signifi-
cant factor for the A–D of carabids by size class, while the main
treatments of tillage × cover crop varied in their effect
(Supplementary Table S4, Fig. 3). In S2, but not S1, year in rota-
tion significantly affected the A–D of small carabids. In S1, the
mean A–D of small carabids was 3.75 ± 0.33, 2.31 ± 0.33 and
3.41 ± 0.94 in years 1, 2 and 3, respectively. In S2, small carabids
increased through the rotation and the mean A–Ds were 0.94 ±
0.23, 1.21 ± 0.21 and 2.55 ± 0.49 in years 1, 2 and 3, respectively.
In S2, the A–D of small carabids was greater in year 3 compared
with years 1 (P< 0.0001) and 2 (P= 0.0020). In S2, the propor-
tional representation of small carabids was intermediate in year
1 (20.5 ± 5.9%), lowest in year 2 (13.4 ± 2.2%) and highest in
year 3 (41.8 ± 5.4%). In S1, neither the main treatments of tillage
nor cover crop significantly affected the A–D of small carabids. In
S2, tillage had a significant effect on the A–D of small carabids, in
which the mean A–D was greater in RT (1.92 ± 0.35) compared
with FT (1.21 ± 0.23), which corresponded to a proportional
representation of 25.8 ± 4.9 and 24.6 ± 4.6% of the population,
respectively.
Year in the rotation had a significant effect on the A–Dof
medium-sized carabids in S1 and S2 (Supplementary Table S4,
Fig. 3). In S1, the mean A–D of medium carabids was 3.21 ±
0.22, 0.31 ± 0. 0.13 and 2.91 ± 0.65 in years 1, 2 and 3, respectively,
and mean A–D was greater in years 1 (P< 0.0001) and 3 (P<
0.0001) compared with year 2. These A–Ds corresponded to
30.7 ± 2.1, 5.1 ± 2.2 and 18.9 ± 3.3% medium carabids in years 1,
2 and 3, respectively. In S2, the mean A–D of medium carabids
was 0.42 ± 0.09, 1.02 ± 0.20 and 0.44 ± 0.18 in years 1, 2 and 3,
respectively, and A–D was greater in year 2 than in years 1 (P
< 0.0262) and 3 (P< 0.0206). These A–Ds corresponded to 8.3
± 2.1, 11.3 ± 2.8 and 5.4 ± 1.4% medium carabids in years 1, 2
and 3, respectively. In S1, but not S2, tillage treatment affected
the A–D of medium carabids. The mean A–D of medium cara-
bids was 2.52 ± 0.50 in FT and 1.76 ± 0.31 in RT, representing
19.7 ± 3.1 and 16.8 ± 2.9%, respectively. In S1, there was a signifi-
cant interaction between tillage and cover crop in which the mean
A–D was 3.46 ± 0.82, 1.58 ± 0.47, 1.40 ± 0.30 and 2.13 ± 0.53 in
the FT × RYE, FT × TIM, RT × RYE and RT × TIM treatments,
respectively. These A–Ds corresponded to 22.3 ± 4.1, 17.2 ± 4.7,
13.5 ± 3.0 and 20.2 ± 4.9%, respectively. In RYE treatments, the
A–D of medium carabids was greater (P= 0.0002) in FT com-
pared to RT. In FT treatments, the A–D of medium carabids
was greater (P= 0.0008) in RYE compared to TIM treatments.
The A–D of large carabids was affected by year in rotation in
S1 and S2 (Supplementary Table S4, Fig. 3). In S1, the mean A–D
of large carabids was 3.77 ± 0.33, 3.29 ± 0.42 and 8.75 ± 1.35 in
years 1, 2 and 3, respectively, and A–D of large carabids was
greater in year 3 than in years 1 (P< 0.0001) and 2 (P< 0.0001).
These A–Ds corresponded to proportions of large carabids of
34.9 ± 2.2, 55.3 ± 5.7 and 57.4 ± 5.1% in years 1, 2 and 3, respect-
ively. In S2, the A–D of large carabids was 3.98 ± 0.55, 7.02 ± 0.92
and 3.38 ± 0.57 in years 1, 2 and 3, respectively, and A–D of large
carabids was greater in year 2 than in years 1 (P= 0.0044) and 3
Table 1. Summary of carabid activity density (A–D) and richness (S) between Starts and treatments
Full tillage Reduced tillage
Carabid Start Total RYE TIM Total RYE TIM Total
A–D 1 1282 394 341 735 259 287 546
2 899 300 247 547 192 160 352
S 1 46 34 31 39 33 33 39
2 473327 38 3331 38
6 Tara Pisani Gareau et al.
(P= 0.0003). These A–Ds represented proportions of large cara-
bids of 71.2 ± 6.6, 74.8 ± 3.6 and 51.9 ± 5.4% in years 1, 2 and 3,
respectively. Neither the main treatments of tillage and cover
crop nor their interactions had a significant effect on the A–D
of large carabids in S1 or S2. However, in S1, the interaction of
year and cover crop affected large carabids. In years 1 and 2,
the A–D of large carabids did not differ between RYE and TIM,
but in year 3 the A–D was greater (P= 0.0070) in RYE (11.88 ±
2.07) than in TIM (5.63 ± 0.86) treatments, representing 57.7 ±
8.1 and 46.1 ± 7.2% large carabids, respectively.
Fig. 2. The A–D of carabid species that showed significant fidelity to particular treatments as determined by Indicator Species Analysis in Starts 1 and 2.
Renewable Agriculture and Food Systems 7
Carabid trophic behavior
Year in rotation and the main treatments of tillage and cover crop
had variable effects on the A–D of carabid feeding guilds
(Supplementary Table S4, Fig. 4). In S1, but not in S2, year in
rotation significantly affected the A–D of carnivores. In S1, the
A–D of carnivorous carabids was 6.56 ± 0.61, 3.04 ± 0.34 and
6.66 ± 0.78 in years 1, 2 and 3, respectively, and the A–D of car-
nivores was greater in years 1 (P< 0.0001) and 3 (P< 0.0001)
compared with year 2. These A–Ds corresponded to proportions
of carnivores of 60.2 ± 3.9, 51.7 ± 4.6 and 47.6 ± 5.0% in years 1, 2
and 3, respectively. In S1, the interaction of year with cover crop
had a significant effect on the A–D of carnivorous carabids in
which the A–D in years 1 and 2 was not different for RYE and
TIM, but in year 3, the A–D of carnivores was greater (P=
0.0330) in RYE (8.44 ± 1.02) compared with TIM (4.88 ± 0.82).
These A–Ds corresponded to proportions of carnivores of 46.3
± 8.5 and 48.8 ± 5.9% in RYE and TIM in year 3, respectively.
In S2, the main effect of cover crop had a significant effect on
the A–D of carnivores in which the A–D in RYE (4.21 ± 0.36)
was greater than the A–D in TIM (2.75 ± 0.46) treatments (P=
0.0021). The proportions of carnivores in S2 were 58.7 ± 3.9 and
44.5 ± 5.5% in RYE and TIM, respectively.
Table 2. Indicator values and significance of Indicator Species Analysis (ISA) for carabid species collected in treatments in Start 1
Indicator value (IV)
Full tillage Reduced tillage
Species (CODE) RYE TIM RYE TIM P
Agonum cupripenne (AGCU) 13 8 13 5 0.9368
Agonum muelleri (AGMU) 29 3 1 1 0.0426
Agonum octopunctata (AGOC) 11 0 3 0 0.5961
Agonum placidum (AGPL) 1 15 3 15 0.5367
Agonum punctiforme (AGPU) 0 2 2 10 0.5955
Anisodactylus sanctaecrucis (ANSA) 25 1 2 2 0.107
Bembidion mimus (BEMI) 9 1 9 1 0.3923
Bembidion quadrimaculatum (BEQU) 18 22 36 21 0.0558
Bembidion rapidum (BERA) 15 10 22 10 0.6077
Chlaenius tricolor tricolor (CHTR) 6 5 13 2 0.6277
Cicindela punctulata (CIPU) 18 13 1 23 0.3477
Clivinia bipustulata (CLBI) 2 2 7 2 1
Clivinia impressifrons (CLIM) 3 3 3 0 1
Colliuris pensylvanicus (COPE) 2 0 5 2 1
Cyclotrachelus furtivus (CYFU) 0 2 0 13 0.4085
Dyschirius globulosus (DYGL) 0 4 23 4 0.1304
Elaphropus incurvus (ELIN) 4 20 8 7 0.4195
Harpalus affinis (HAAF) 0 3 3 3 1
Harpalus compar (HACO) 11 2 0 5 0.5947
Harpalus herbivagus (HAHE) 12 1 5 11 0.7357
Harpalus pensylvanicus (HAPE) 13 23 19 23 0.9144
Harpalus rubripes (HARU) 1 1 6 6 1
Patrobus longicornis (PALO) 13 2 3 1 0.4525
Poecilus chalcites (POCH) 31 13 26 19 0.3331
Poecilus lucublandus (POLU) 15 10 16 15 0.9798
Pterostichus melanarius (PTME) 5 5 1 5 1
Pterostichus mutus (PTMU) 0 11 3 0 0.5971
Scarites quadriceps (SCQU) 12 13 25 14 0.4733
Stenolophus comma (STCOm) 29 4 0 4 0.0628
Trechus quadristriatus (TRQU) 9 9 1 1 0.9488
Species that occurred in less than three plots were excluded from the analysis. Abundance values in the matrix were not transformed or relativized, because the procedure relativizes the
data. P-values were derived from Monte Carlo randomization tests and show the statistical significance of the maximum indicator value (bolded species have P-values < 0.10).
8 Tara Pisani Gareau et al.
In both S1 and S2, year in rotation significantly affected the
A–D of granivorous carabids (Supplementary Table S4, Fig. 4).
In S1, the A–D of granivores was 0.75 ± 0.10, 0.79 ± 0.11 and
1.81 ± 0.36 in years 1, 2 and 3, respectively, and was greater in
year 3 than in years 1 (P= 0.0126) and 2 (P= 0.0099). These
A–Ds corresponded to 7.7 ± 1.0, 12.8 ± 1.7, and 12.4 ± 1.9%
granivores in years 1, 2 and 3, respectively. In S2, the A–Dof
granivores was 0.59 ± 0.15, 4.02 ± 0.50 and 0.61 ± 0.13 in years
1, 2 and 3, respectively, and was greater in year 2 than in years
1(P< 0.0001) and 3 (P< 0.0001). The proportions of granivores
were 12.2 ± 2.8, 44.3 ± 4.0 and 10.4 ± 2.7% in years 1, 2 and 3,
respectively. In S2, the mean A–D of granivores was greater in
RT (2.29 ± 0.50) than in FT (1.19 ± 0.27) treatments. These
A–Ds corresponded to 22.9 ± 4.1 and 21.6 ± 4.2% in RT and FT,
respectively. In S2, there was a significant interaction of tillage
with cover crop for the A–D of granivorous carabids in which
the A–D of granivores was greater (P= 0.0005) in RT (2.51 ±
0.65) than in FT (0.92 ± 0.29) in RYE treatments, but there was
no difference in A–D of granivores between RT and FT in TIM
treatments. In RYE, proportions of granivores were 24.0 ± 5.3%
in RT and 14.4 ± 4.2% in FT.
In both S1 and S2, year in rotation affected the A–D of omniv-
orous carabids (Supplementary Table S4, Fig. 4). In S1, the A–D
of omnivores was 3.33 ± 0.61, 2.08 ± 0.34 and 6.59 ± 0.78 in years
Table 3. Indicator values and significance of Indicator Species Analysis (ISA) for carabid species collected in treatments in Start 2
Indicator values (IV)
Full tillage Reduced tillage
Species (CODE) RYE TIM RYE TIM P
Agonum cupripenne (AGCU) 1 1 21 1 0.1054
Agonum muelleri (AGMU) 19 0 2 0 0.1724
Agonum punctiforme (AGPU) 2 0 17 4 0.2196
Anisodactylus sanctaecrucis (ANSA) 11 1 3 7 0.7033
Bembidion obtusum (BEOB) 1 4 9 4 0.9452
Bembidion quadrimaculatum (BEQU) 19 12 13 24 0.6179
Bembidion rapidum (BERA) 2 7 19 0 0.2901
Calathus gregarius (CAGR) 11 3 0 0 0.5995
Chlaenius emarginatus (CHEM) 2 7 3 0 0.8942
Chlaenius tricolor tricolor (CHTR) 6 0 19 1 0.2134
Cicindela punctulata (CIPU) 4 9 10 9 0.9928
Cicindela sexguttata (CISE) 0 2 2 8 0.8974
Clivinia bipustulata (CLBI) 1 11 2 7 0.6023
Clivinia impressifrons (CLIM) 6 1 1 6 1.0000
Cyclotrachelus furtivus (CYFU) 1 8 8 6 0.9668
Dyschirius globulosus (DYGL) 0 0 13 2 0.4127
Elaphropus incurvus (ELIN) 5 6 10 12 0.9158
Harpalus affinis (HAAF) 1 1 22 0 0.1144
Harpalus compar (HACO) 1 5 8 8 0.8498
Harpalus herbivagus (HAHE) 1 0 0 28 0.0342
Harpalus pensylvanicus (HAPE) 1 0 0 28 0.3439
Harpalus rubripes (HARU) 1 21 5 9 0.2799
Patrobus longicornis (PALO) 0 2 2 8 0.8970
Poecilus chalcites (POCH) 37 5 40 7 0.0082
Poecilus lucublandus (POLU) 18 3 35 21 0.0992
Pterostichus melanarius (PTME) 0 11 6 24 0.1450
Scarites quadriceps (SCQU) 9 2 15 6 0.5493
Stenolophus comma (STCOm) 2 0 14 1 0.1922
Trechus quadristriatus (TRQU) 13 0 6 8 0.5995
Species that occurred in less than three plots were excluded from the analysis. Activity–density values in the matrix were not transformed or relativized, because the procedure relativizes the
data. P-values were derived from Monte Carlo randomization tests and show the statistical significance of the maximum indicator value (bolded species have P-values < 0.10).
Renewable Agriculture and Food Systems 9
1, 2 and 3, respectively, and was greater in year 3 than in years 1
(P= 0.0108) and 2 (P< 0.0001). The proportions of omnivores
were 32.0 ± 3.4, 35.4 ± 4.8 and 40.1 ± 5.0% in years 1, 2, and 3,
respectively. In S2, the A–D of omnivores was 0.50 ± 0.11, 2.02
± 0.25 and 2.74 ± 0.48 in years 1, 2 and 3, respectively, and was
greater in years 2 (P< 0.0001) and 3 (P< 0.0001) than in year
1. The proportions of omnivores were 11.9 ± 3.2, 23.3 ± 2.6 and
43.1 ± 4.5% in years 1, 2 and 3, respectively. In S1, the interaction
of year and cover crop was a significant effect for the A–Dof
omnivores. There was no difference in A–D of omnivores between
cover crop treatments in years 1 and 2, but the A–D of omnivores
was greater (P= 0.0032) in RYE (9.63 ± 2.00) than in TIM (3.56 ±
0.70) treatments in year 3. In year 3, the proportion of omnivores
was 44.4 ± 8.7% in RYE and 35.7 ± 5.2% in TIM. In S2, the inter-
actions of year with tillage and tillage with cover crop were signifi-
cant for the A–D of omnivorous carabids. The A–D of omnivores
was not different between RT and FT treatments in years 1 and 2
but was greater (P= 0.0136) in RT (3.56 ± 0.55) than in FT (1.92
± 0.69) treatments in year 3. In year 3 in S2, the proportion of
omnivores was 43.0 ± 5.9% in RT and 43.1 ± 7.1% in FT. The
A–D of omnivores in RYE treatments did not differ between
RT and FT; however, in TIM treatments, the A–D of omnivores
was greater (P= 0.0067) in RT (2.51 ± 0.57) than in FT (1.11 ±
0.27) treatments. In TIM in year 3, the proportion of omnivores
was 33.5 ± 6.5% in RT and 26.6 ± 5.2% in FT.
Effects of environmental variables
Carabid A–D and species richness
Environmental variables had a significant effect on carabid A–D
and species richness, and these effects differed between S1 and
S2 (Table 4). Four environmental variables explained the variation
in total carabid A–D. In S1, soil moisture was a positive predictor,
Cu was a negative predictor, and together explained 44% of the
variation in carabid A–D. In S2, soil moisture, annual weed dens-
ity and perennial weed density were all positive predictors and
explained about 27% of variation in A–D. Eight environmental
variables explained variation in carabid species richness
(Table 4). In S1, soil Cu and annual SDR were negative predictors,
and soil pH, CEC and P were positive predictors and explained
66% of the variation in carabid species richness. In S2, K was a
negative predictor, and soil moisture and annual weed density
were positive predictors and explained 33% of the variation in
carabid species richness.
Carabid assemblage
RDA constrained by cover crop × tillage treatments for each of the
years in the rotation and each of the experimental Starts indicate
the associations among treatment, environmental variables and
carabid beetle species occurring in >25% of samples and with a
fit of >20% to the model. In S1, year 1, nine carabid species
met the inclusion rules, and the explanatory variables accounted
for 26.8% of the variation in A–D. Axis 1 accounted for 17.3%
of the variation, whereas Axis 2 accounted for 9.5% (Fig. 5a).
TIM treatments were associated with the annual number of dis-
turbances, Agonum placidum (Say), Cyclotrachelus furtivus
(LeConte), B. quadrimaculatum,H. pensylvanicus,Elaphropus
incurvus (say) and Trechus quadristriatus (Schrank). RYE treat-
ments were associated with perennial weed density, annual
SDR, A. muelleri,P. chalcites and Agonum cupripenne (Say). In
S1, year 2 (Fig. 5b), six species met the inclusion rules and the
model explained 26.5% of variation. Axis 1 explained 17.9%
and Axis 2 explained 7.6% of the variation, respectively. Both
TIM treatments occurred in the same quadrant of the biplot
and were associated with perennial weed density, annual number
of disturbances, SDR and C. punctulata. T. quadristriatus was
associated with FT × RYE treatments. P. lucublandus and SDR
were associated with Axis 1. B. quadrimaculatum,A. cupripenne
and Clivinia bipustulata (Fabricius) were associated with RT ×
RYE. In year 3, the constrained model accounted for 23.9% of
the variation in the carabid community with axes 1 and 2 explain-
ing 15.3 and 8.6% of the variation, respectively. In year 3, FT ×
TIM and RT × TIM occurred in the same quadrant as perennial
weed density. RT × RYE was associated with Dyschirius globulosus
(Say) and P. lucublandus (Fig. 5c). FT × RYE was associated with
SDR, Anisodactylus sanctaecrucis,S. comma,H.herbivagus and B.
rapidum.
In Start 2, the variation in the carabid community explained by
the RDA declined over the 3 yr of the experiment (Fig. 5d–f). In
year 1, the constrained model explained 28.0% of variation. Axis 1
explained 17.0%, while Axis 2 explained 11.0% of the variation
(Fig. 5d). No variables or species were associated with RT ×
TIM. H. rubripes was associated with FT × TIM. Perennial weed
density, annual number of disturbances and SDR were associated
with RYE treatments. B. rapidum and A. cupripenne were asso-
ciated with perennial weeds and RT × RYE, T. quadristriatus
and P. chalcites were closely associated with the annual number
of disturbances and SDR, and A. muelleri was associated with
FT × RYE. In year 2 of S2, the RDA explained 23.2% of the vari-
ation in the carabid community, with Axes 1 and 2 explaining
14.8 and 9.1% of the variation, respectively (Fig. 5e). The FT treat-
ments were co-located in the same quadrant and were not asso-
ciated with any carabid species or environmental variables. Axis
1 was associated with the annual number of disturbances, SDR
and soil pH. Axis 2 was associated with perennial weeds and
RT × TIM, H. herbivagus and Pterostichus melanarius (Illiger).
H. pensylvanicus and C. furtivus were associated with RT treat-
ments, and P. lucublandus,Chlaenius tricolor (Dejean), C. punctu-
lata and P. chalcites were associated with RT × RYE. In year 3
(Fig. 5f), the RDA constrained by treatment accounted for
20.9% of the explained variation in the carabid community, and
Axes 1 and 2 explained 11.6 and 9.2% of the variation, respect-
ively. TIM treatments were co-located in the quadrant with peren-
nial weeds but no carabid taxa. The four carabid taxa with >20%
fit to the model were associated with RT treatments, SDR, annual
number of disturbances and perennial weeds. RT × TIM was asso-
ciated with P. lucublandus and B. quadrimaculatum.RT×RYE
was associated with H. affinis and Scarites quadriceps (Chaudoir).
Carabid beetle guilds: size class
Eight environmental variables contributed to the variation in the
A–D of carabids categorized by size class (Table 4). In S1, annual
SDR, weed species richness and annual weed density were nega-
tive predictors, and soil S and Zn were positive predictors and
together explained 49% of the variation in the A–D of small car-
abids. Soil moisture was a positive predictor, and soil S and per-
ennial weed density were negative predictors and explained 49%
of the variation in the A–D of medium carabids. Soil moisture
and annual SDR were positive predictors and soil Cu was a nega-
tive predictor for the A–D of large carabids, and together
explained 39% of the variation. In S2, soil pH and sentinel insect
infection by Metarhizium were positive predictors and explained
37% of the variation in the A–D of small carabids. Soil K was a
negative predictor and annual SDR was a positive predictor of
10 Tara Pisani Gareau et al.
medium carabids and together explained 14% of the variation in
A–D. Sentinel insect infection by Metarhizium, perennial weed
density and weed species richness were negative predictors, and
annual weed density was a positive predictor for large carabids
and explained 45% of the variation in A–D.
Carabid beetle guilds: trophic behavior
Nine environmental variables contributed to the variation in A–D
of carabid trophic guilds (Table 4). In S1, soil moisture was a posi-
tive predictor and soil Cu was a negative predictor, and together
explained 38% of the variation in A–D of carnivores.
Approximately 27% of the variation in granivores was explained
by soil EC and Cu as negative predictors and LOI-OM as a posi-
tive predictor. Perennial weed density was a negative predictor
and soil moisture was a positive predictor together explaining18%
of the variation in the A–D of omnivores. In S2, 26% of the vari-
ation in the A–D of carnivores was explained by annual weed
density as a positive predictor and annual SDR and sentinel insect
infection by Metarhizium as negative predictors. Approximately
74% of the variation in granivores was explained by the annual
number of disturbances, sentinel insect infection by
Metarhizium and soil Cu as negative predictors and perennial
weed density and soil moisture as positive predictors. Annual
SDR and annual weed density were positive predictors and
explained 40% of the variation in omnivorous beetles.
Discussion
Tillage
We expected that large-sized carabids would be most negatively
affected by tillage intensity, because several studies have reported
a reduction in body size with increasing frequency and intensity of
disturbances (Blake et al., 1994; Coombs et al., 1996; Ribera et al.,
2001; Tsiafouli et al., 2015; Hanson et al., 2016). However, tillage
was not a significant effect for large-sized beetles, while small-
sized beetles were significantly more active in RT treatments.
Fig. 3. Mean annual carabid activity–density according to size class in the four cover crop × tillage treatments in each year of the experiment. FT = full tillage, pri-
mary tillage using a moldboard plow. RT = minimum tillage, primary tillage using a chisel plow. Rye = biculture of cereal rye and red clover in year 1. Tim = sod cover
crop of timothy followed by hairy vetch in year 1.
Renewable Agriculture and Food Systems 11
The higher numbers of small beetles in RT plots were contrary to
our hypothesis, although Holland and Luff (2000) mention that
small carabids may prefer RT systems. We also expected grani-
vores to be more active in RT treatments. Herbivorous ground
beetle species often prefer less disturbed habitats, such as field
margins with grass (Birkhofer et al., 2014; Winqvist et al.,
2014), likely in response to plant-based resources. In their study
comparing the effects of moldboard plowing, chisel plowing
and rotary tillage to an undisturbed control on carabids,
Shearin et al.(2007) found that rotary tillage and moldboard
plowing reduced granivore A–D by 52 and 54%, respectively,
but that granivore A–D after chisel plowing was similar to the
undisturbed control. Similarly, we found that granivore A–D
was significantly higher in treatments that used chisel plow tillage
(RT) in comparison to moldboard plow (FT), although the effect
was greater (a 94% increase) in S2 than in S1 (only a 3% increase).
Increasing land-use intensity can benefit carnivorous ground bee-
tles (Caballero-López et al., 2012; Birkhofer et al., 2014; Hanson
et al., 2016); however, tillage was not a significant effect for carni-
vores, or for omnivores.
Cover crop
Cover crop was only significant for carnivores in S2. The carniv-
orous carabids that showed a preference for RYE plots, evident by
RDAs and IVs, included P. chalcites, a large-sized carabid of open
habitats, A. muelleri and A. cupripenne, medium-sized carabids
that are common in open habitat, and B. rapidum, a small-sized
carabid that is common around wetland habitat. Cereal rye was
planted in rows, which may have created a more suitable habitat
for these carnivores in comparison to the denser timothy/clover
sod. Eyre et al.(2013) found that within an organic crop rotation,
A–D of carabids was limited by a grass/clover mixture in com-
parison to cereal crops. Cereal rye may also have continued to
provide resources, such as prey or habitat structure, to P. chalcites
in the subsequent years after the cultivation of cereal rye, as the
Fig. 4. Mean annual carabid activity–density categorized by trophic guilds in the four cover crop × tillage treatments in each year of the experiment. FT = full tillage,
primary tillage using a moldboard plow. RT = minimum tillage, primary tillage using a chisel plow. Rye = biculture of cereal rye and red clover in year 1. Tim = sod
cover crop of timothy followed by hairy vetch in year 1.
12 Tara Pisani Gareau et al.
association of P. chalcites with RYE treatments continued even
into the second (soybean) and third (corn) year of the rotation.
Volunteer cereal rye was present in years 2 and 3 in treatment
plots (Smith et al., 2011). RDAs revealed that cover crop is repre-
sented by the primary axis in the first year of the rotation in both
starts. In S1, H. pensylvanicus,B. quadrimaculatum,A. placidum
and E. incurvus are associated with the TIM treatment, while in
S2 H. rubripes is associated with TIM. This pattern is also evident
in the IVs. With the exception of E. incurvus, which is common in
wet habitat, the other species are characterized as open habitat
species. Without the association of environmental variables with
the TIM treatment in year 1, it is difficult to say what is driving
those relationships. Because the relationship is not consistent
across starts for the dominant carabids, there are likely other fac-
tors involved that were not measured in the study.
Environmental variables
Many studies have examined the relationship between biotic and
abiotic factors and carabid beetles (Thiele, 1977; Holland et al.,
Table 4. Statistical values for forward selection multiple linear regression analysis for significant environmental variables (explanatory variables) and Carabidae
activity-density, species richness (S) and guilds (response variables)
Start 1 Start 2
Indicator r
2
(adj)
for model Environmental variables Estimate Pr
2
(adj)
for model Environmental variables Estimate P
Carabid A–D 0.441 Soil moisture 0.147 <0.0001 0.274 Soil moisture 0.1313 0.0008
Copper −0.218 0.0268 Annual weed density 0.001 0.0131
Perennial weed density 0.011 0.0297
Carabid S 0.658 Cu −2.867 0.0001 0.332 Soil moisture 0.663 0.0008
Annual SDR −0.029 0.0005 K −0.024 0.0161
pH 4.334 0.0021 Annual weed density 0.005 0.0174
CEC 0.804 0.0077
P 0.085 0.0378
Size class
Small 0.489 Annual SDR −0.076 <0.0001 0.373 Soil pH 0.227 0.0014
Weed spp. richness −0.004 0.0001 Sentinel insect infection rate 0.003 0.0081
Sulfur 0.041 0.0085
Annual weed density −0.001 0.0366
Zn 0.105 0.0596
Medium 0.493 Soil moisture 0.049 0.0001 0.141 K −0.001 0.0039
Sulfur −0.025 0.0017 Annual SDR 0.001 0.0581
Perennial weed density −0.002 0.0335
Large 0.387 Soil moisture 0.051 0.0003 0.447 Sentinel insect infection rate −0.493 0.0001
Annual SDR 0.003 0.0008 Annual weed density 0.003 0.0014
Cu −0.101 0.0145 Perennial weed density −0.006 0.0016
Weed spp. richness −0.043 0.0034
Trophic group
Carnivore 0.381 Soil moisture 0.035 0.0003 0.256 Annual weed density 0.0004 0.0008
Cu −0.097 0.0026 Annual SDR −0.0012 0.0014
Sentinel insect infection rate −0.0030 0.0256
Granivore 0.265 EC −0.001 0.0016 0.735 Annual No. disturbances −0.026 <0.0001
Cu −0.069 0.0061 Perennial weed density 0.004 0.0001
LOI-SOM 0.138 0.0074 Soil moisture 0.026 0.0021
Sentinel insect infection rate −0.004 0.0021
Cu −0.129 0.0147
Omnivore 0.181 Perennial weed density −0.003 0.0493 0.404 Annual SDR 0.001 0.0005
Soil moisture 0.026 0.0557 Annual weed density 0.001 0.0043
Analyses based on [log (A–D + 1)] transformation of A–D.
Renewable Agriculture and Food Systems 13
2007; Schirmel et al., 2016). The results of our RDAs suggest that
the structure of the carabid community is dynamic through the
crop rotation. In each year, multiple environmental variables
were influential in structuring the carabid community.
Environmental variables with consistent negative or positive asso-
ciations with informative carabid species included the intensity of
soil disturbance, number of soil disturbances and perennial weed
density. Using multiple regression analysis, we also identified sev-
eral environmental variables (soil moisture, weed measures,
annual SDR, soil Cu concentration and infection of sentinel
insects by Metarhizium) that were significant predictors of vari-
ability in carabid A–D, species richness and guild.
Soil moisture
Soil moisture at our site on pitfall sample dates ranged from 12 to
21% and was one of the most frequent positive predictors for car-
abids. In S1, soil moisture was a positive predictor for A–D,
medium- and large-sized beetles, carnivores and omnivores, and
in S2, it was a positive predictor for A–D, species richness and
granivores. Soil moisture is a key factor affecting habitat selection
among carabids (Thiele, 1977) and can drive carabid larval sur-
vival, distribution, diversity and community composition
(Holopainen et al., 1995; Holland et al., 2007). Holland et al.
(2007) examined the effect soil moisture patterns in two arable
fields on the distribution and abundance of nine carabid species
and found stable spatial patches for six species related to soil
moisture and a significant linear relationship between emergence
densities and soil moisture for three species. Soil moisture content
can be influenced in organic systems by increasing SOM. A
meta-analysis of 60 published studies demonstrated that a 1%
increase in soil organic carbon on average increased the available
water capacity by 1.16%, with a larger increase in sandy soils
(Minasny and McBratney, 2018). Incorporating organic materials
such as animal manure and finished compost into the soil
increases SOM and thus water holding capacity. Straw mulches
also add to SOM and increase soil moisture by reducing evapor-
ation; however, straw mulch can deter carabids that prefer open
habitat. For example, in an experiment to determine the effects
of an organic cover crop-based RT system, B. quadrimaculatum
was more abundant in standing cereal rye compared to cereal
rye mulch created by terminating the cover crop with a roller-
crimper (Rivers et al., 2017).
Weeds
Weed measures were one of the most common significant predic-
tors for carabid A–D and guild composition in multivariate ordi-
nations and multiple regressions. Weeds affect carabids via
resource-mediated effects, e.g., by providing seeds and pollen or
herbivorous prey, and structure-mediated effects, e.g., by provid-
ing shelter and favorable microclimate (Pavuk et al., 2009; Diehl
et al., 2012; Kulkarni et al., 2015). Many carabid species are sig-
nificant consumers of post-dispersal weed seeds (Kulkarni et al.,
2015), and even species considered highly carnivorous have
been documented to feed on weed seeds (Hunter, 2009;
Fig. 5. Biplots representing results of partial redundancy analyses constrained by treatments for carabid species with supplementary environmental variables for
years 1 (a), 2 (b) and 3 (c) of Start 1 and 1 (d), 2 (e) and 3 ( f ) of Start 2. For S1, constrained axes 1 and 2 account for 17.3 and 9.5%; 17.9 and 7.6%; and 15.3 and
8.6% of the variation in years 1, 2 and 3, respectively. For S2, constrained axes 1 and 2 account for 17.0 and 11.0%; 14.8 and 9.1%; and 11.6 and 9.2% of the
variation in years 1, 2 and 3, respectively. We used an inclusion rule of occurrence in 25% of pitfall samples for the inclusion of a carabid species in the analysis,
and a fit of 20% to the model for inclusion of species and supplementary variables to be included on the biplot. Abbreviations for carabid taxa are presented in
Supplementary Table S3.
14 Tara Pisani Gareau et al.
Lundgren, 2013). Perennial weed density was a positive predictor
of granivore A–D in S1. Carabid beetle body size is among the
major determinants of weed seed preferences (Honek et al.,
2007), with small carabid species preferring small seeds and
large carabid species preferring larger seeds (Gaines and
Gratton, 2010). As expected, annual weed density was a positive
predictor for carabid A–D and most guilds in S2. However, con-
trary to our prediction, perennial weed density and weed species
richness were negative predictors for large carabids in S2. We
expected that the association of large carabids would be greater
in plots with perennial weeds, as perennial habitats are generally
more supportive of larger and slower carabids.
Disturbance frequency and intensity
Tillage and other soil management operations can have a pro-
found effect on the environment for carabid beetles and other
soil organisms, influencing, e.g., arthropod prey, weed flora and
seed distribution, and vegetation cover as well as abiotic proper-
ties. Our study demonstrates that nominal tillage treatments
may not result in a simple and consistent difference in disturb-
ance frequency and intensity, especially if plots are managed for
the agronomic value of the cash crop. For example, because of
weather and soil conditions, we had to implement additional sec-
ondary cultivations in S2 soybeans to facilitate crop emergence in
the RT × TIM treatment.
Annual SDR and the number of disturbances were significant
environmental variables for the A–D of some carabid species and
guilds. The RDAs indicated species with significant responses to
soil disturbance in each year of the two Starts. In S1, the intensity
of soil disturbance was a negative predictor for carabid species
richness and small carabids, and, unexpectedly, a positive pre-
dictor for large carabids. RDAs revealed that the A–D of our
most frequently captured species, the large carnivore P. chalcites,
was positively related to the intensity of soil disturbance in year 1
of both Starts, but not in years 2 and 3, which may have been due
to the field preparation of cover crops in the fall before the rota-
tion year. Spring breeders that overwinter as adults may be pro-
tected from fall tillage activities by burrowing deep in the soil
profile and escaping direct disturbance (Holland and Luff,
2000). Alternatively, P. chalcites is more active in conventionally
tilled fields as found in other studies (Menalled et al., 2007;
O’Rourke et al., 2008).
In S2, the intensity of disturbance was a positive indicator for
medium carabids and omnivores, and a negative indicator for car-
nivores. The frequency of disturbance was a negative predictor for
granivores in S2. In RDAs, the small omnivores B. quadrimacula-
tum and T. quadristriatus, as well as the medium granivore, H.
herbivagus, were positively associated with disturbance vectors.
Large carnivores with a negative association with the vectors for
disturbance in S2 included C. tricolor, and the dominant species,
C. punctulata and P. lucublandus. Unlike in year 1, P. chalcites
was negatively associated with vectors for disturbance in year
2. The inclusion of this species as a significant responder to dis-
turbance in opposing ways at different times in multivariate ordi-
nations suggests that it is insensitive to disturbance. The
consistent inclusion of soil disturbance indicators as significant
variables for guilds and species in multivariate analyses suggests
that future studies that aim to compare the effects of soil manage-
ment treatments on Carabidae and other soil-associated arthro-
pods should quantify disturbance associated with specific
practices in an ecologically meaningful way. We chose to quantify
disturbance prior to a pitfall sample by intensity and frequency
within the season and accumulated over the rotation. However,
there may be other disturbance variables, such as time since last
disturbance or disturbance during the breeding season, that we
did not include that are important to the A–D, reproduction
and survivorship of carabids.
Soil copper
We measured several soil minerals, including Cu, S and Zn. In S1,
Cu was a negative predictor for A–D, richness (S), large-sized spe-
cies, carnivores in S1 and for granivores in both Starts. Copper
had a direct acute toxic effect on mortality of larval Pterostichus
cupreus L. and locomotor behavior of adults produced from sur-
viving larvae was impaired (Bayley et al., 1995). These authors
suggested that such changes in locomotor behavior are likely to
reduce carabid fitness under field conditions. In our site, Cu con-
centrations were within normal ranges for crop production, and
were likely increased by the application of animal manure and
manure-based compost used to provide soil fertility. In organic
production systems, animal manures are very commonly used
to manage soil fertility. The negative association between Cu
and carabids at our site suggests that the broader relationship
between soil Cu and epigeal arthropod predators should be
examined.
Entomopathogenic fungi
Cosmopolitan EPF in the genus Metarhizium (Metschnikoff)
Sorokin (Hypocreales: Clavicipitaceae) occurs primarily in soil
and have a broad arthropod host range and are well-adapted to
agricultural systems (Meyling and Eilenberg, 2007). In S2, infec-
tion of sentinel insects by Metarhizium was a positive predictor
for small-sized species, and a negative predictor for large-sized
species, carnivores and granivores. Some practices or environmen-
tal conditions may result in increases of infection by pathogens
and survival of eggs, larvae, pupae or adults (Holland and Luff,
2000), but relatively few studies have focused on the association
between agricultural practices and epigeal predators and EPF.
Steenberg et al.(1995) found a high prevalence of infection by
EPF, from 19 to 50%, in carabid larvae from lucerne and cabbage
fields in Denmark. Specifically, they noted infection of larvae of
the granivore, Amara fulva (Müller), Harpalus sp. and ‘other car-
abids’. At our study site, we detected Metarhizium more fre-
quently in the FT × TIM treatment and this fungus was
negatively associated with soil moisture, organic matter, and
zinc, sulfur and copper concentrations (Jabbour and
Barbercheck, 2009). Although we did not directly observe or
test for fungal infections of carabids, it is interesting that soil
moisture was a positive predictor for carabids but a negative pre-
dictor for Metarhizium. This pattern could reflect either lower
mortality of carabids in areas of high moisture and low
Metarhizium prevalence, or avoidance of beetles of areas or con-
ditions that favor Metarhizium (Fry et al., 2019).
Conclusion
We tested the effects of two levels of tillage intensity (moldboard
plow vs chisel plow) and two different cover crop mixes (a rye cer-
eal with hairy vetch vs a sod-forming timothy grass with clover)
on carabid beetles. We used several carabid response variables
including total A–D, richness, individual species, size classes
and trophic behavior. While tillage had a significant effect on
granivores and small beetles, both preferring the RT treatment,
cover crop treatments had a significant effect on carnivores and
Renewable Agriculture and Food Systems 15
in particular on P. chalcites, which was found in greater numbers
in the RYE treatment, which provided a more open habitat and
potentially other resources that persisted into the third year of
the rotation. Our research also shows how the level of disturbance
is more complex than reflected by nominal treatments. Our RT
treatments generally experienced a similar frequency of distur-
bances, but lower intensity of disturbance compared with full till-
age treatments over the 3-yr transition period. The frequency and
intensity of disturbance negatively affected A–D for some carabid
guilds and species, but not all. P. chalcites, e.g., was positively
associated with other environmental variables, such as weed dens-
ity, soil moisture, pH and soil copper. The habitat affinity of agri-
culturally adapted carabid species is likely the result of a
combination of environmental variables that make a habitat suit-
able based on the species phenology and behavior (Thiele, 1977;
Holland and Luff, 2000). We found that management practices
that encourage soil moisture support a diverse weed community,
and reduce the frequency and intensity of disturbance support
total carabid A–D, richness and the majority of guilds, which
may increase biological control services during the transition to
organic production.
Supplementary material. The supplementary material for this article can
be found at https://doi.org/10.1017/S1742170519000255
Acknowledgements. This research would not have been possible without Dr
Randa Jabbour, who led the pitfall data collection from the plots. We thank
S. Harkcom, D. Heggenstaller, V. Houck, B. Jones, S. Kinneer, C. Nardozzo,
D. Sandy and S. Smiles for providing technical assistance, and many under-
graduate students who diligently sorted insects. We gratefully acknowledge
the advice provided by our advisory board: C. Altemose, L. Garling,
J. Moyer, B. Snyder, K. Yoder, P. Yoder, A. Ziegler and L. Zuck. Funding
for this research was provided by the USDA NIFA Competitive Grants
Program-IPM-ORG-112.E.
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