Content uploaded by Augusto Loni
Author content
All content in this area was uploaded by Augusto Loni on Oct 21, 2019
Content may be subject to copyright.
1
© The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America.
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Community Ecology
Ground Beetle (Coleoptera: Carabidae) Assemblages and
Slug Abundance in Agricultural Fields Under Organic and
Low-Input Conventional Management Within a Long-Term
Agronomic Trial in CentralItaly
Elisabetta Rossi,1,3, Daniele Antichi,2, Augusto Loni,1 Roberto Canovai,1
Massimo Sbrana,2 and Marco Mazzoncini2
1DAFE Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto, 80, 56124 Pisa, Italy, 2CiRAA Centre for
Agri-environmental Research ‘Enrico Avanzi’, via Vecchia di Marina, 6, 56122 San Piero a Grado, Pisa, Italy, and 3Corresponding author,
e-mail: elisabetta.rossi@unipi.it
Subject Editor: Richard Redak
Received 10 April 2019; Editorial decision 12 September 2019
Abstract
Inside a long-term agronomic trial aimed at evaluating the effects of organic and low-input conventional management
systems on soil fertility and arable crop production, we selected six fields bordered by hedgerows, three under each
management system. Here, we analyzed the carabid assemblages and the slug abundance. Samplings took place in
five different periods, across 1 yr of observations. The carabid abundances were similar in organic and conventional
fields. The Shannon–Wiener diversity index (H’) showed a higher value in the conventional fields, although in the
organic fields, a higher number of species were observed. The multivariate analysis described similar carabid
communities, but excluding the period factor, it showed a significant influence of the management system. There
was no difference between the captures of traps placed along the hedgerow and in the middle, whereas in the
conventional fields, the hedgerow traps captured a higher number of specimens, showing a role of the hedgerow
as carabid reservoir. The slugs were present mainly while green manure was grown on the organic fields where also
Poecilus cupreus Linné, 1758 (Coleoptera: Carabidae)was captured abundantly.
Key words: Carabid, community, agricultural management system, hedgerow, biodiversity
Carabids are efcient bioindicators in terrestrial ecosystems because
of their adaptability and ability to colonize almost all terrestrial
habitats and geographical locations, their quick response to envir-
onmental changes, the ease in collecting them, and their relatively
stable taxonomy. They are also useful organisms in agroecosystems
due to their role as predators of crop insect pests (Kotze etal. 2011,
Pizzolotto et al. 2018) and slugs, thus reducing their populations
(Fusser etal. 2016).
However, the risk of misusing data on carabid assemblages as
environmental indicators has been stressed (Gobbi and Fontaneto
2008) when considering only species richness without a contextual-
ization of their ecologicalrole.
In temperate areas, the differences among carabid communities
are frequently used as an indicator in the evaluation of the impact
caused by different agricultural practices, crops, and surrounding
habitats (Holland and Luff 2000, Albertini etal. 2017, Lemic etal.
2017). However, carabid populations seem to be relatively constant
over time (Holland 2002) in arable crops, as shown from the data
obtained in long-term trials carried out in arable elds (Luff 1982).
Habitat diversication within cultivated elds can signicantly in-
uence the quantity and quality of carabid fauna in agroecosystems.
Field margins and their management as well as agroecological in-
frastructures have an inuence on the qualitative and quantitative
composition of carabid populations; thus, edges can be an important
tool for carabid conservation (Rouabah etal. 2015). The presence
of hedgerows, in particular, is known to affect the diversity and dis-
tribution of Carabids, as some species are typically related to the
hedges, whereas others prefer the cropped areas, have a weak prefer-
ence for the hedge habitat, or are randomly distributed between the
eld and the hedge (Fournier and Loreau 1999).
Carabids have frequently been used to compare the biodiversity
in organic and conventional management systems (Kromp 1989,
Purtauf et al. 2005, Gomiero etal. 2011, Legrand et al. 2011).
Much evidence shows how agroecological practices can mean that
organic systems have less of an impact on carabid habitats than
conventionalones.
Environmental Entomology, XX(XX), 2019, 1–11
doi: 10.1093/ee/nvz119
Research
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
Some soil management practices such as reduced tillage (with
or without soil inversion; Shearin et al. 2007) or cover cropping
(Shearin etal. 2008) can considerably inuence the effects of organic
management on carabid biodiversity. Normally, low-input practices
make organic systems overall more eco-friendly and sustainable than
conventional ones, although the sustainability is important not only
from a short-term perspective, but also taking into account a long
timeline. In this view, long-term trials, despite the investment in man-
power, help us to understand the ecology of agricultural systems.
Carabids can be a useful tool to monitor the effects of different man-
agement systems also in long-term trials (Legrand etal. 2011).
Carabids are active generalist predators of slugs, which could
represent an important resource in their diet (Bohan etal. 2000).
Terrestrial slugs live worldwide in temperate and tropical regions.
Some species are important agricultural pests in Europe, North
America, New Zealand, some parts of Australia and Central America
(Howlett 2012). Mild and damp climate, but also agronomic prac-
tices as no-tillage (Douglas and Tooker 2012), herbaceous eld
borders (Fusser etal. 2016), the overwintering green crops, or or-
ganic management (Vernava etal. 2004) can signicantly promote
infestations.
Little information is known about the economic importance of
slugs as crop pests in Italy, but their damage is reported on many
crops (Santini 2000).
This article describes the carabid assemblages and the slug abun-
dance monitored in six experimental elds as part of a long-term
agronomic trial 15 yr after it started. The elds were all in the same
size with a hedgerow on one side and managed under two different
systems (organic and conventional management). This situation is
interesting due to the contiguity of the elds and the length of the
management systems.
The focus was on the following hypotheses:
1) the carabid community structures will differ under the two man-
agement systems;
2) the hedgerows have a different role in carabid distribution de-
pending on the presence of an overwintering cover crop in or-
ganic elds or bare soil in the conventional elds; and
3) there is a relationship between the slug abundance and the
carabid assemblages.
Materials and Methods
MASCOT Long-Term Trial—ExperimentalSite
Since 2001, the Centre for Agri-environmental Research ‘E. Avanzi’
(CiRAA), S. Piero a Grado, Pisa, Italy (latitude 43°40′N, longi-
tude 10°18′E) hosts the MASCOT (Mediterranean Arable Systems
COmparison Trial) trial (Barberi and Mazzoncini 2006), a long-term
experiment still ongoing, focusing on the comparison of organic and
conventional management systems.
Its main objective is to compare soil fertility (in the broader
sense of term), crop performance, and agroecological aspects for
a 5-yr stockless arable crop rotation under organic and a low-in-
put conventional management system. The crop rotation included
maize (Zea mays L.), common wheat (Triticum aestivum L.), sun-
ower (Helianthus annuus L.), pigeon bean (Vicia faba var. minor
Beck), and durum wheat (Triticum turgidum subsp. durum Desf.).
In the organic system, green manures were winter grown in between
winter wheat and spring crops (i.e., maize and sunower; Ciaccia
et al. 2017). The elds in the organic system were supplied with
commercial organic fertilizers (i.e., pelleted dried staple manure),
whereas the conventional elds were supplied with mineral fertil-
izers. The weed control was mechanical in the organic system (ex-
tine harrowing and inter-row cultivation) and chemical/mechanical
(inter-row cultivation for row crops) in the conventional system. The
main and secondary tillage methods were the same for both systems
(Mazzoncini etal. 2010, 2015).
CiRAA elds are included in the Migliarino San Rossore
Massaciuccoli Park territory and classied as transition areas of the
UNESCO Biosphere Reserve ‘Selva Pisana’. This location imposes a
low-input agriculture also in the conventional system.
Experimental Fields and Their Management
Six rectangular experimental elds were chosen among the plots
of the MASCOT trial (Fig. 1). Their sizes were about 30× 300 m
each one, and they were delimited by a hedgerow and a ditch along
the longest sides. Three were under organic management and three
were under conventional management. The hedges contained a mix-
ture of local species: Crataegus monogyna Jacq., Cornus sanguinea
L., Ligustrum vulgare L., Lonicera xylosteum L., Prunus spinosa
L., and Rhamnus cathartica L.and were about 1.5 m deep. In the
2015/2016 season, in the organic elds, a mixture of hairy vetch
(Vicia villosa Roth.) and barley (Hordeum vulgaris L.) was grown as
green manure between September 2015 and April 2016. The conven-
tional elds, on the other hand, were kept bare until the following
spring. Seedbeds were prepared for maize in the two systems by two
passes of a rotary harrow on 28 April and 5 May 2016, respectively.
In the conventional elds, one spray of glyphosate (900g/ha of ac-
tive ingredient) was performed on 28 April to reduce the number of
weeds that had grown over the winter. In Table 1, the sequence of
crops in organic and conventional elds isshown.
Across the sampling periods until the beginning of July 2016,
the elds bordering the other sides of the hedgerows were cropped
with common wheat in organic or conventional system. In the period
from wheat harvest (4 July 2016)to September 2016, these elds
were kept bare (with wheat residues retained on soil surface) and
untilled.
Animal Sampling
Carabids
Carabids were sampled by pitfall traps consisting of plastic 250-ml
jars, which were buried up to the opening, and covered with a plastic
dish, supported by four aluminum sticks and 5cm high from the
trap border. Each trap was baited with 100ml of white vinegar and
10g of NaCl. Sixteen traps were placed in two parallel rows (eight
traps per row) about 15 m from each other along the median axis of
the eld and along the edge, tangential to the hedgerows. The trap
distance along the row was 30 m (Fig. 1). The samplings covered
a period of 10 mo from 6 November 2015 to 12 September 2016.
This interval was ranked in ve different periods, as indicated in
Table 1: each period included 2 or 4wk of sampling. The ve peri-
ods were chosen according to the crop development, focusing on the
periods with likely higher presence of carabids and slugs and with
contrasting weather conditions to have a realistic representation of
the population dynamics across the year. The rst period was set
around the sowing and establishment of the green manure mixture
sown in the organic elds. The second period covered 2wk before
the termination date of the green manure mixture in the organic
system. The third, fourth, and fth periods covered, respectively,
early establishment, vegetative growth, and harvest time of the corn
crop following the green manure mixture in the organic elds and
the bare soil in the conventional elds.
2 Environmental Entomology, 2019, Vol. XX, No. XX
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
The trap content was removed after 2 d and sieved; the carabids
were collected and stored in 70% alcohol until their classication.
Carabids were identied to species level with the specic keys for
Italian carabids (Brandmayr etal. 2005; Pesarini and Monzini 2010,
2011). Specimens were stored in the Department of Agriculture,
Food and Environment (DAFE) entomological collection.
Slugs
Slug samplings were performed with eight commercial mat traps
(Anti-Limaces Ciblage, De Sangosse) aligned in the middle of each
experimental eld, adjacent to the pitfall traps to maximize any
abundance difference between organic and conventional elds,
assuming that close to the hedgerows the habitats were more similar.
We were more interested in studying the abundance of slugs in re-
lationship to carabids as their potential predators than describing
their community structure so that the classication was carried out
at family level without distinguishing between young and mature
individuals. Atrap was made with a multi-layer material, with alu-
minum on one side and absorbent tissue on the other (0.25 m2 sur-
face, 0.5× 0.5 m size). This design allows the trap to keep water
beneath (i.e., in the absorbent tissue facing downwards) and reect
solar radiation on top (i.e., on aluminum side facing upwards), thus
preventing air temperature rising so high to kill or deter slugs using
the traps as shelter along the day. The mat traps were soaked in
Fig. 1. Field arrangement of MASCOT trial. Triangles show the experimental fields where the pitfall and mat traps were placed. For each field that is not part of
our experiment, the main crop during the sampling periods of carabids and slugs is indicated. Label GM–M indicates the rotation of green manure and maize in
organic fields, whereas BS–M indicates the bare soil before maize, in conventional fields. Dots in detail indicate the position of pitfall traps.
Table 1. Sampling dates and crops grown in the experimental fields
Week of sampling Periods Sampling dates Management
Organic Conventional
1 1 6 Nov. 2015 Barley and vetch Bare
2 13 Nov. 2015 Barley and vetch Bare
3 19 Nov. 2015 Barley and vetch Bare
4 27 Nov. 2015 Barley and vetch Bare
5 2 4 Apr. 2016 Barley and vetch Bare
611 Apr. 2016 Barley and vetch Bare
7 3 25 May 2016 Corn Corn
8 8 June 2016 Corn Corn
9 4 4 July 2016 Corn Corn
10 11 July 2016 Corn Corn
11 25 July 2016 Corn Corn
12 1 Aug. 2016 Corn Corn
13 5 5 Sept. 2016 Corn Corn
14 12 Sept. 2016 Corn Corn
Environmental Entomology, 2019, Vol. XX, No. XX 3
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
water for half an hour before being installed in the eld. The traps
were removed from the ground after 48h at the same time of pitfall
emptying and the slugs sheltering under the mat traps were collected
in plastic jars and then counted and classied in the lab at the family
level following the key of Cameron etal. (1983). The captures were
relevant only in organic elds. Here during the periods in which the
slugs were captured, a correlation analysis was performed between
the slug abundance and that of the whole captures of carabids. This
same analysis was repeated selecting the most represented carabid
species. The analysis was performed using the ‘agricolae’ package for
R (Mendiburu 2015).
Estimate of Carabid Biodiversity
Data on captures were used to estimate biodiversity under the two
management systems. The species richness was calculated using the
two nonparametric estimators Chao1 and Chao2 in data sets from
the organic and conventional elds. Chao1 is one of the most ef-
fective abundance-based estimators, basing its calculations rstly on
singletons and doubletons, i.e., the number of species represented for
just one or two individuals across all the samples (Basualdo 2011).
Chao2 is the corresponding incidence-based estimator, counting sin-
gles and duplicates, i.e., species that are present only in one or two
samples, respectively (Chao and Chiu 2016). The Shannon–Wiener
diversity (H’) and Pielou’s evenness (J’) indexes were calculated
considering all the captures for the organic and conventional elds
(Magurran 1988).
Statistical Analysis
Multivariate Analysis
Data on carabid captures were organized into a raw data matrix with
all samples in columns, and species and their relative abundance in
rows. Asimilarity matrix was created calculating the Bray–Curtis
similarity index between each pair of samples. Atwo-dimensional
graphical representation, i.e., the nonmetric multidimensional scale
(NMDS), was performed on this similarity matrix and the null
hypothesis (i.e., no differences exist among the groups of carabid
population samples) was tested by the nonparametric permuta-
tional, multivariate analysis of variance (Permanova). We veried the
homogeneity of the data dispersion by the permutational analysis of
data dispersion (Permdisp).
We adopted two different experimental designs. In the rst one, a
mixed design with three factors, ‘Management’ (Mn; xed factor with
two levels, Organic, Org, and Conventional, Con), ‘Trap position’ (Tp;
xed factor with two levels, Edge, Ed, or Middle of the eld, Md), and
the random factor ‘Period’ (Pe; with ve levels, 1–5), was adopted. The
second was a crossed design with a two-xed factors, Mn (two levels,
Org and Con) and Tp, (two levels, Ed or Md). We collapsed the time
factor by cumulating all sampling dates to obtain a nal, global view
of the inuence of management and trap position on the carabid com-
munity structure. AP value of 0.01 was chosen as the signicancelevel.
We also performed an analysis of the similarity percentage of
species contribution (SIMPER) considering the two experimental de-
signs (Clarke and Warwick 2001). In conventional elds, the analysis
was performed for highlighting the species mostly contributing to
the dissimilarity between the groups Con–Md and Con–Ed.
Permanova A+ for Primer software package was used for all ana-
lyses (Anderson etal. 2008).
Chi-Square
Comparison
The comparison among the capture abundances was carried out
using the interactive calculation tool for chi-square tests of goodness
of t and independence (Preacher 2001).
Results
Carabids
During the trial, the traps captured 14,507 carabids in total, with 7,319
specimens captured in the organically managed elds and 7,188 in the
conventional ones (Table 2). The differences between the two abun-
dances were not statistically different (χ
2=1.18; df=1; P=0.28). The
captures were higher the second, fourth, and fth periods, despite the
fourth and fth periods consisted of only two sampling weeks. There
were a total of 54 species, 48 from the organic elds and 44 from the
conventional ones. The majority of captured species were zoophagous
and macropterous. The species with the highest captures were Poecilus
Table 2. Total number of Carabids trapped in the organic and conventional fields during the samplingdates
Sampling periods Sampling dates Capture number Species number
Management Tot. no. Management Tot. no.
Org Con Org Con
1 6 Nov. 2015 227 247 474 20 23 30
13 Nov. 2015 90 83 173 11 11 17
19 Nov. 2015 107 62 169 16 9 17
27 Nov. 2015 79 10 89 8 4 8
24 Apr. 2016 1,586 297 1,883 17 20 23
11 Apr. 2016 538 560 1,098 11 18 19
3 25 May 2016 158 592 750 12 17 20
8 June 2016 459 113 572 19 11 23
4 4 July 2016 274 203 477 17 14 20
11 July 2016 423 389 812 16 18 23
25 July 2016 911 671 1,582 19 18 22
1 Aug. 2016 839 1,166 2,005 15 17 21
5 5 Sept. 2016 1,052 1,895 2,947 15 15 17
12 Sept. 2016 576 900 1,476 13 15 16
Tot. no. 7,188 a 7,319 a 14,507 48 44 54
Same letters represent not signicant differences (χ
2=1.18; df=1; P=0.28).
4 Environmental Entomology, 2019, Vol. XX, No. XX
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
cupreus (Linnaeus), followed by Pseudoophonus rupes (De Geer),
Brachinus immaculicornis Dejean and Pterostichus melas Dejean, re-
spectively. Poecilus cupreus and P.rupes accounted for 52% of total
captures (Supp Table 1 [online only]).
Table 3 shows the captures of these two species divided for
the sampling period and trap position factors. The captures of
P.cupreus in the border traps and those in the middle were signi-
cantly different (χ
2=987.2; df=1; P<0.001) in both organic and
conventional elds. Poecilus cupreus was particularly abundant in
the second sampling period and in the middle traps of organic elds.
For P.rupes, the difference between the captures in the edge and
middle traps was signicantly different (χ
2=42.9; df=1; P<0.001)
only in conventional elds, with a higher number of specimens
trapped on the edge and a peak in the fth period of sampling.
Estimate of Carabid Biodiversity
Both the Shannon–Wiener diversity and the Pielou’s evenness indexes
were lower in the organic than the conventional elds (H’=1.834 vs
2.066 and J’=0.471 vs 0.546, respectively) even if the total number
of species (49 vs 44)and specimens (7,319 vs 7,188) were higher in
the organic elds.
These data matched consistently with the lower evenness meas-
ured for the organic elds than the conventional ones. This might
be reasonable due to the population peak of P.cupreus during the
second period of samplings (Table 3), which produced an unbal-
anced evenness of this species. For this reason, we calculated the di-
versity indexes without considering P.cupreus (Supp Table 2 [online
only]), showing that both diversity indexes were higher in organic
than in conventional elds.
Carabid Species Richness Estimators
Nonparametric estimators Chao1 and Chao2 reached an asymptote
in both organic and conventional elds, with a different number of
estimated species. In the organic elds, a higher number of species is
expected than in the conventional elds (62 vs 52). However, in both
management options, the number of species observed was lower than
the estimated ones: this suggests that a higher number of species could
be hosted both in organic and conventional elds (Fig. 2A and B).
Multivariate Analysis
Three-Factor ExperimentalDesign
In the graph of the NMDS analysis, the samples organized on the
basis of the Mn and Tp factors were not grouped into different
clusters (Fig. 3A). In contrast, taking into account the Pe factor, or-
dination showed denite clouds of data corresponding to the ve
sampling periods (Fig. 3B).
The sample distribution described by the NMDS analysis was
supported by the Permanova, which found no signicant differ-
ences between groups of samples on the basis of the Mn factor
(P= 0.0192, df =1, Unique perms.= 9,926) and the Tp factor
(P=0.6851, df= 1, Unique perms. = 9,943), without signicant
interaction Mn×Tp (P=0.1922, df=1, Unique perms.=9,954).
However, highly signicant differences were found for the Pe factor
(P=0.0001, df=4, Unique perms.=9,891). An analysis of the
dispersion of samples conrmed the homogeneous dispersion of
samples, without inuencing the Permanova results (F=0.42276;
df=1; df2= 422; P (perm) =0.574). The Pe factor produced the
highest signicance value between groups, also determining a
strong inuence on the interactions with other factors (Mn×Pe
P= 0.0001, df=4, Unique perms.=9,977; Tp× Pe P =0.0001,
df=4, Unique perms.=9,886; Mn×Tp×Pe P=0.0001, df=4,
Unique perms.=9,891). Given that Pe is a random factor, we only
considered its contribution to the variation among samples exclud-
ing the residuals (Supp Table 3 [online only]). We also applied
Permanova to analyze separately the captures of the rst two peri-
ods and those of the last three periods of sampling. This is because
in the rst two sampling periods, the crops in the conventional and
organic elds were not identical (due to the particular features of
the cropping system: green manure crop in organic elds vs bare
soil in conventional elds). The results are reported in Supp Tables
S4 and S5, where Pe factor was the only signicant factor, whereas
Mn and Tp factors were not signicant.
Two-Factor ExperimentalDesign
The NMDS analysis performed on a two-factor design and based
on the Mn factor, produced two clouds of data with the samples of
the organic elds grouped on the upper-left of the graph, and the
Table 3. Captures of Poecilus cupreus and Pseudoophonus rufipes divided according to trap position (edge or middle) in the sampling
period and under the organic and conventional management systems
Sampling periods Sampling dates Poecilus cupreus Pseudoophonus rupes
Org. Con. Org. Con.
E M E M E M E M
1 6 Nov. 2015 0 0 0 0 10 14 39 25
13 Nov. 2015 0 0 0 0 6 3 7 1
19 Nov. 2015 0 0 0 1 6 3 10 1
27 Nov. 2015 0 0 0 0 0 0 0 0
24 Apr. 2016 44 1,382 9 73 2 2 7 0
11 Apr. 2016 26 355 10 48 5 1 20 0
3 25 May 2016 59 1 1 0 3 0 198 2
8 June 2016 181 4 0 0 1 4 12 1
4 4 July 2016 47 90 4 1 1 1 69 1
11 July 2016 108 137 13 10 4 2 70 3
25 July 2016 218 311 50 85 34 77 131 72
1 Sept. 2016 65 318 53 67 53 137 277 219
5 5 Oct. 2016 6 19 15 9 285 266 649 266
12 Oct. 2016 34 6 3 4 164 137 239 125
Tot. no. 788a 2,623b 158a 298b 574a 647a 1,728a 716b
Environmental Entomology, 2019, Vol. XX, No. XX 5
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
conventional ones forming two clouds on the lower-left and on the
middle of the graph (Fig. 4A).
The same analysis considering the Tp factor showed two loose
clouds with the edge trap samples on the left and the middle trap
samples on the right (Fig. 4B). The two outlier samples on the right
part of Fig. 4A and B represent a failure of the sampling (due to the
accidental loss of traps), which nevertheless did not affect the results
of the NMDS ordination as conrmed by Permanova.
The Permanova analysis conrmed this visualization of the sam-
ples with signicant differences among groups of samples on the
basis of the Mn (P=0.0001, df=1, Unique perms.=9,922) factor
as well as the Tp (P=0.0027, df=1, Unique perms.=9,936) factor
with a signicant interaction Mn×Tp (P=0.0001, df=1, Unique
perms.=9,938). The distribution of the samples was not affected
by a nonhomogeneous sample dispersion (deviation from centroid
for Mn factor: F=5.13; df1=1; df2=30; P (perm)=0.05; for Tp
factor: F=5.13; df1=1; df2=30; P (perm)=0.05).
Based on the signicant interaction between the Mn and Tp fac-
tors, we performed the corresponding pairwise test. In line with the
NMDS graph, sample groups from the organic and conventional
elds were different both within level Md of factor Tp (P=0.0002;
Perm.=5,072) and within level Ed (P=0.0002; Perm.=5,048).
Sample groups of the Md and Ed traps were not signicant
within the level Org (P = 0.18, Perm.= 5,088), but were signi-
cantly different within the level Con of the Mn factor (P=0.0005;
Perm.=4,998). Due to the clear-cut separation of the conventional
samples into two clouds (Fig. 4A), we repeated the NMDS analysis
by combining the Mn and Tp factors. In this case, the conventional
samples on the edge compared with those in the middle position
were easily distinguishable (Fig. 5). By combining the Mn and Tp
factors and recalculating the diversity indexes (Table 4) emerged the
important role of the hedgerow in the conventional elds, given that
it supported a notably higher number of species and specimens.
SIMPER Analysis
In the three-factor design, the average Bray–Curtis similarity cal-
culated between all pairs of samples, considering the management
system factor, was 24.67 in the organic group and 25.23 in the con-
ventional one (Supp Table 6 [online only]). Pseudoophonus rupes
and P.cupreus together cumulated almost 50% of the average simi-
larity in organic elds. Pseudoophonus rupes contributed 23.08%
with the highest ratio similarity/standard deviation (Sim/SD=0.61),
meaning that this species was well represented and distributed across
all samples of the group. Poecilus cupreus had a higher percentage
contribution to the average similarity (25.31%), however with a
lower ratio similarity/standard deviation (Sim/SD=0.53), meaning
a less homogeneous distribution among samples. Pseudoophonus
rupes and P.melas typied the groups of samples in the conven-
tional elds, contributing about 60% of the average similarity.
Pseudoophonus rupes accounted for 38.52% and was well dis-
tributed among the samples (Sim/SD= 0.81), whereas P.melas ac-
counted for 20.50% with a ratio Sim/SD of0.62.
The same analysis was repeated for the combined factors Mn and
Tp in the two-factor design. Poecilus cupreus, P.rupes, B.immac-
ulicornis, B.crepitans, N.brevicollis, and P.melas typied both the
Fig. 3. Nonmetric multidimensional scale analysis. Same symbols in each graph represent samples grouped on the basis of the same factor. (A) Management;
(B) sampling period.
Fig. 2. Rarefaction curves showing observed (Sobs, black line) and estimated species richness using Chao1 (dark gray line) and Chao2 (light gray line) estimators
in organic (A) and conventional (B) fields.
6 Environmental Entomology, 2019, Vol. XX, No. XX
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
middle and edge traps in the organic elds giving account of about
70% of average similarity of samples (Supp Table 7 [online only])
without producing separation between the two groups. The spe-
cies P.rupes, B. immaculicornis, B.crepitans (L.), P.cupreus, and
P.melas typied the middle trap samples in the conventional elds,
whereas the species P. rupes, P.melas, N.brevicollis (Fabricius),
and P. niger (Shaller), typied the population of the traps near to
the hedges in the same elds. Dissimilarity analysis performed be-
tween groups Con–Md and Con–Ed showed that P.niger, P.melas,
N.brevicollis, and C.fuscipes (Göeze) were the species that showed
the main percentage contribution to the dissimilarity between the
two groups (Supp Table 8 [online only]).
Slugs
Table 5 shows the total number of slugs captured with the mat traps
in the experimental elds and divided according to each sampling
period. No slugs were captured in the summer, due to the dry soil
conditions. Limacidae resulted the most captured family, whereas sig-
nicantly less captures were observed for Milacidae and Arionidae.
The slugs were more abundant in the organic elds where the
green manure cover made the habitat conditions suitable for slug
survival, locomotion, and reproduction until the cover crop has been
plowed into the soil (end of April 2016). However, no damage on
the vetch-barley cover crop was observed. The correlation between
the slug captures and the total number of carabids reached a value of
0.74. By selecting the most represented species typifying the organic
habitat, according to simper analysis, we observed as P. cupreus
population was the only species showing high correlation (δ=0.95)
with slug abundance (Table 6). In the conventional elds, only six
slugs were captured across the sampling periods.
Discussion
In this work, we investigated the composition of carabid fauna and
slug abundance in elds under different management systems, in a
long-term agronomic trial carried out near Pisa (Italy).
The carabid abundance was not signicantly different under the
two management systems. Poecilus cupreus and P.rupes were the
main species captured. This result is consistent with the data col-
lected across Europe by other authors (Porhajašová et al. 2014,
Rouabah etal. 2015, Brygadyrenko 2016). These two species have
a wide environmental adaptability (Porhajašová etal. 2014) and are
considered as typical representatives of the carabid fauna of open
habitats and agroecosystems (Tuf etal. 2012, Fusser etal. 2016). The
prevalence of both these macropterous species (as most of the cap-
tured species) could be related to their better dispersal ability, which
makes them suitable in the ecosystems that experience disturbance
(Langraf etal. 2017). In particular, organic elds experienced more
disturbance as tillage was used for weed control.
The high number of carabid species captured with a very low
number of specimens (one or two individuals), suggests that they
could play an important role in replacing the loss or reduction of
another species with the same functional role (Naeem 1998, Mori
etal. 2013). Two species, Asaphidion festivum and Carabus granula-
tus interstitialis, are included in the regional Red List of Tuscany as
rare species or in danger of extinction (Sforzi and Bartolozzi 2001),
and both were represented in our samples. In particular, A.festivum
(11 specimens) was found only in the organic elds, whereas 18
Fig. 4. Nonmetric multidimensional scale analysis. In each graph, the same symbols represent samples grouped on the basis of the same factor. (A) Management;
(B) trap position.
Fig. 5. Nonmetric multidimensional scale analysis carried out on captures
simultaneously taking into account management and trap position.
ConMd=middle traps in fields with conventional management; ConEd=edge
traps in fields with conventional management; OrgMd = middle traps in
fields with organic management; OrgEd= edge traps in fields with organic
management.
Table 4. Diversity index calculated by grouping the species by
combining the two Mn (management) and Tp (trap position; Md:
middle, Ed: edge) factors
Combined factors S N J’H’
Org–Md 40 4.851 0.45 1.65
Org–Ed 35 2.468 0.59 2.09
Con–Md 33 2.413 0.55 1.93
Con–Ed 41 4.775 0.53 1.98
S (number of species); N (number of specimens); J’ (Pielou’s evenness); H’
(Shannon–Wiener diversity index).
Environmental Entomology, 2019, Vol. XX, No. XX 7
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
specimens of C.granulatus interstitialis were found in the conven-
tional elds and only three in the organic ones. Their presence sug-
gests the hypothesis of an agroecosystem rich in biodiversity, where
also rare species can nd enough resources. Rare species could be a
positive side effect of the low-input agriculture, prolonged over time
in the experimental site, although the stability of their presence has
to be conrmed by future samplings.
The Shannon–Wiener index values were a little higher in
the conventional than in the organic elds, although the total
number of species was higher in the organic than the conventional
elds. This difference can be reasonably attributed to the peak in
P.cupreus, which altered the evenness. In fact, by excluding this
species from the H’ calculation, the index was higher in the or-
ganic elds.
Chao1 and Chao2 indexes estimated a potential to host 10 spe-
cies more in the organic elds than in the conventional ones sug-
gesting a higher resource availability of organic elds.
Poecilus cupreus is a polyphagous predator, which is also
common in arable-ecosystems throughout Europe (Langmaack etal.
2001). It is an iteroparous species, with a spring–summer breeding
activity (Matalin 2007). Its biological cycle matched well with our
peak of captures. Our data revealed a particular spatial and temporal
distribution of this species: the highest number of captures was con-
centrated in the middle traps of organic elds during the second sam-
pling period. These results are consistent with Thomas etal. (2001),
who reported a preferential aggregation of this species in patches
within the crop, far from the border with hedgerows. However, they
are not in line with the results of Fournier and Loreau (1999) and
Rouabah etal. (2015), who prevalently captured this species along
the edges of the elds. These discrepancies could be reasonably due
to the complexity of the interactions among the factors, which are
known to drive the spatial distribution of carabids, and specically,
of P.cupreus. In particular, the causes of the opposite results could
be sought in the differences between the situations, such as the age
of the hedge, the diversity of crops, and the level of input of the man-
agement system.
Pseudoophonus rupes is a common species in European
agro-biocenoses with summer–autumn breeding activity. In accord-
ance with Matalin (1997), our captures showed a peak in the au-
tumn and a second, minor peak during the summer samplings. In
the conventional elds, the captures mainly occurred in the border
traps close to the hedgerows. These results support the ndings by
Thomas etal. (2001), who trapped carabids in winter cereal elds
with hedgerows near Bristol (United Kingdom). In the organic elds,
P. rupes captures were lower: we speculate that this occurrence
could be due to the higher soil disturbance in these elds during the
spring period, whereas the higher presence of weeds in these elds
could result in a change of its distribution inside them, being the spe-
cies zoospermophagous.
The community structure, described by a three-factor design ana-
lysis (which takes into account the factor management, period, and
trap position), showed that the carabid assemblages were similar in
the two management systems, but changed only in relation to time.
This evidence was conrmed by the results obtained collapsing the
captures of the rst two periods and those of the second three peri-
ods: again, the comparison between organic and conventional elds
did not show any signicant difference. These results showed the
similarity of the two communities.
However, in the two-factor design, the differences in community
structure, due to the management systems, emerged quite clearly.
This is reasonably due to an overall view of data obtained by col-
lapsing the time factor: this allowed to highlight the global effect of
small differences in each single period.
As regards the inuence of hedgerows on captures, the conven-
tional elds showed marked differences in the species composition
and quantity of captures, thus highlighting the positive effect of
hedges in biodiversity richness. The crucial role of hedgerows as an
ecological infrastructure in agroecosystems and their importance in
connectivity is well known (Burgio etal. 2015, Sutter etal. 2017).
On the opposite, this effect was not observed in the organic elds,
probably because of the presence from the autumn to the early
spring of an undisturbed green manure cover, which produced a less
Table 6. Pearson correlation among the entire Carabid population and the most abundant Carabid species and slug captures
Carabids Tot. no. Brachinus crepitans Poecilus cupreus Brachinus immaculicornis Pterostichus melas Pseudoophonus rupes
0.75 −0.29 0.95 −0.51 −0.44 −0.31
Table 5. Slugs trapped in the sampling periods in the two cropping systems
Date of samplings Period Organic elds Tot. no. Conventional elds Tot. no.
Limacidae Milacidae Arionidae Limacidae Milacidae Arionidae
6 Nov. 15 1 0 8 0 8 0 0 0 0
13 Nov. 15 3 7 5 15 0 0 0 0
19 Nov. 15 2 10 0 12 0 0 0 0
27 Nov. 15 0 3 6 9 0 0 0 0
4 Apr. 16 2 48 0 9 57 1 0 0 1
11 Apr. 16 105 1 2 108 0 0 0 0
25 May 2016 3 2 0 1 3 0 0 0 0
8 June 2016 0 0 0 0 0 0 0 0
4 July 2016 4 0 0 0 0 0 0 0 0
11 July 2016 0 0 0 0 0 0 0 0
25 July 2016 0 0 0 0 0 0 0 0
1 Aug. 2016 0 0 0 0 0 0 0 0
5 Sept. 2016 5 0 0 0 0 0 1 1 2
12 Sept. 2016 0 0 0 0 0 0 0 0
Tot. no. 160 29 23 212 1 1 1 3
8 Environmental Entomology, 2019, Vol. XX, No. XX
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
disturbed environment between the border and the middle of the
elds. This hypothesis is consistent with the results of Varchola and
Dunn (2001) who observed a seasonal movement of carabids from
the hedgerow to the inner part of a corn eld, with the gradual in-
crease of the ground cover by the plants. The green manure cover
reasonably increased the suitable habitat for carabids reducing the
spatial competition among species.
According to the SIMPER analysis, P.cupreus and P.rupes were
the most represented species in the organic and conventional elds,
respectively. The uneven distribution of P. cupreus was highlighted
by the lower ratio similarity/standard deviation.
In our study, P. niger, P. melas, N. brevicollis, and C. fuscipes
have been found along eld edges, in line with other papers (Nazzi
etal. 1989, Thomas etal. 2001, Ranjha and Irmler 2014, Rouabah
etal. 2015). Such species contributed the highest percentage to the
dissimilarity between groups Con–Md and Con–Ed.
The slug assemblage samplings showed that in the organic elds,
the population was much more abundant than in the conventional
elds. The cover crop reasonably explained this event, although the
subsequent dry summer season drastically reduced their mobility.
This reduced the potentially negative effects on the following crops
as already described in areas with rainy climate, from Vernava etal.
(2004) and Snyder et al. (2016). The trend of slug captures have
a weak correspondence to the whole carabidofauna sampled in
the same periods, but it corresponded with the peak of P. cupreus
captures observed in the organic elds. Poecilus cupreus is a gen-
eralist predator, which includes slug eggs in its diet as showed by
Oberholzer and Frank (2003) under lab conditions. Poecilus cupreus
is a spring-breeder, and its potential feeding activity on slug eggs
may represent an interesting biological controlling factor. The high
correlation obtained between slugs trapped and P.cupreus presence
in organic elds, even if only with an explorative value, could be
consistent with the hypothesis of an ecological response of this spe-
cies to the presence of slugs in the elds. This has been demonstrated
for P. melanarius, which was attracted by the slug chemical cues
(McKemey et al. 2004, El-Danasoury and Iglesias-Piñeiro 2018).
Further eld studies would be necessary to support with certainty
the hypothesis of the same attraction on P. cupreus. However, in
organic elds, the agroecosystem (and the predators, in particular)
seems to have promptly responded to the sudden increase of a po-
tential pest (as the increase of P. cupreus population might suggest),
probably supported by adjacent habitats, such as hedgerows (Fusser
etal. 2016, 2017), which could work as carabid reservoir.
Conclusions
Our samplings took place in various contiguous elds as part of
a long-term agronomic trial, which started in 2001. In this work,
we explored the effects of long-term management systems on the
carabid assemblage and the slug abundance. Although the sampled
elds under the two management systems were close together and
the conventional system was not really intensive, we nevertheless
noted a difference in carabid assemblages, when the samples were
compared without taking into account the sampling period. So the
hypothesis of an inuence of management on the carabid popula-
tion emerged conrming the positive role of organic management in
terms of biodiversity.
The green manure, beyond its positive agronomic role on soil fer-
tility, represented an important habitat resource for carabids, due to
its effects of soil green cover and hosted, at the same time, potentially
harmful species as the slugs. However, the richness of agroecosystem
biodiversity of predatory species can be a resource to contrast their
infestation.
The hedgerows demonstrated their positive role as a biodiver-
sity reservoir in the conventional system, where an overwintering
cover crop was grown. This fact conrms the importance of these
ecological infrastructures in carabid conservation and their role in
supporting ecosystem services.
Finally, our data support once more, the reliability and suitability
of carabids as sensitive bioindicators also at local scale.
SupplementaryData
Supplementary data are available at Environmental Entomology
online.
Supp Table S1. List of Carabids captured in pitfall traps: dominance
values (Dom) are calculated according to Tischler (1949); Org: cap-
tures in organic elds; Con: Captures in conventional elds; Seas.
breed (season breeding: Spr, spring; Aut: autumn); Diet, Z: zoopha-
gous; S: spermophagous; ZS: zoospermophagous); Wings, M: mac-
ropterous, B: brachipterous; P: pteridimorphic; chorotypes (Chor)
were dened according to Vigna Taglianti (2005).
Supp Table S2. Shannon–Wiener diversity and Pielou’s evenness
indexes for captures in the organic and conventional elds, calcu-
lated excluding data on Poecilus cupreus.
Supp Table S3. Estimates of components of variation on the
three-factor mixed design (Pe, random factor).
Supp Table S4. Periods 1 and 2: Permanova analysis carried out on
data of captures in the elds under organic and conventional man-
agement systems during the rst two sampling periods.
Supp Table S5. Periods 3, 4, and 5: Permanova analysis carried out
on data of captures in the elds under organic and conventional
management systems during the sampling periods 3, 4, and5.
Supp Table S6. Similarity percentages—species contribution. Factor
group: Mn, management.
Supp Table S7. Similarity percentages—species contribution factor
group combined: type of management (Mn: Con, Org) and trap pos-
ition (Tp: Md, Ed).
Supp Table S8. Dissimilarity percentages—species contribution
factor group combined: management and trap position factors.
Acknowledgments
The authors wish to thank the Ministero delle Politiche Agricole Alimentari
e Forestali (MiPAAF) and the FP7-ERA-Net CORE Organic Plus consortium,
which nanced the project FERTILCROP (2014–2017), thus enabling this
work to be carried out. The authors also wish to thank the eld and lab staff
of the Centre for Agro-Environmental Research ‘Enrico Avanzi’, University of
Pisa, who provided technical and logistical support, managed the experimental
site, and helped in the sample processing. The authors are grateful to the re-
viewers for their excellent revision, which strongly improved the manuscript.
ReferencesCited
Albertini,A., R.Pizzolotto, and R.Petacchi. 2017. Carabid patterns in olive
orchards and woody-semi-natural habitat: rst implications for conserva-
tions biological control against Bactrocera oleae. BioControl 62: 71–83.
Anderson, M. J., R.N. Gorley, and K.R. Clarke. 2008. Permanova + for
Primer: guide to software and statistical methods. PRIMER-E, Plymouth,
United Kingdom.
Bàrberi,P., and M.Mazzoncini. 2006. The MASCOT (Mediterranean Arable
Systems COmparison Trial) long-term experiment (Pisa, Italy), pp. 1–14. In
J. Raupp, C. Pekrun, M. Oltmanns and U. Köpke, (eds.) Long-term eld ex-
periments in organic farming. ISOFAR Scientic Series, Verlag, Berlin (DE).
Basualdo,C.V. 2011. Choosing the best non-parametric richness estimator
for benthic macroinvertebrates databases. Rev. Soc. Entomol. Argent. 70:
27–38.
Environmental Entomology, 2019, Vol. XX, No. XX 9
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
Bohan,D.A., A.C.Bohan, D.M.Gleen, W.O.C.Symondson, C.W.Wiltshire,
and L.Hughes. 2000. Spatial dynamics of predation by carabid beetles on
slugs. J. Anim. Ecol. 69: 367–379.
Brandmayr,P., T. Zetto, and R.Pizzolotto. 2005. Coleotteri Carabidi per la
valutazione ambientale e la conservazione della biodiversità. Manuale op-
erative, vol. 34, pp. 151–185. APAT, Roma, Italy.
Brygadyrenko,V.V. 2016. Evaluation of ecological niches of abundant species
of Poecilus and Pterostichus (Coleoptera: Carabidae) in forests of steppe
zone of Ukraine. Entomol. Fenn. 27: 81–100.
Burgio, G., D. Sommaggio, M. Marini, G.Puppi, A. Chiarucci, S. Landi,
R. Fabbri, F. Pesarini, M. Genghini, R. Ferrari, et al. 2015. The inu-
ence of vegetation and landscape structural connectivity on butteries
(Lepidoptera: Papilionoidea and Hesperiidae), Carabids (Coleoptera:
Carabidae), Syrphids (Diptera: Syrphidae), and Sawies (Hymenoptera:
Symphyta) in Northern Italy Farmland. Environ. Entomol. 44:
1299–1307.
Cameron,R.A.D., N.B.Jackson, and B.Eversham. 1983. A eld key to the
slugs of the British Isles. Field Studies J. 5: 807–824.
Chao,A., and C.H.Chiu. 2016. Nonparametric estimation and comparison
of species richness, pp. 1–11. In eLS (ed.). John Wiley & Sons, Ltd,
Chichester, United Kingdom.
Ciaccia, C., F. Ceglie, F.Tittarelli, D. Antichi, S. Carlesi, E. Testani, and
S. Canali. 2017. Green manure and compost effects on N-P dynamics
in Mediterranean organic stockless systems. J. Soil Sci. Plant Nutr. 17:
751–769.
Clarke,K. R., and R. M. Warwick. 2001. Change in marine communities:
an approach to statistical analysis and interpretation, 2nd ed. Primer-E,
Plymouth, United Kingdom.
Douglas, M. R., and J.F. Tooker. 2012. Slug (Mollusca: Agriolimacidae,
Arionidae) ecology and management in no-till eld crops, with an em-
phasis on the mid-Atlantic region. J. Integr. Pest Manag. 3: C1–C9.
El-Danasoury,H., and J. Iglesias-Piñeiro. 2018. Predation by polyphagous
carabid beetles on eggs of a pest slug: potential implications of climate
change. J. Appl. Entomol. 142: 340–348.
Fournier, E., and M. Loreau. 1999. Effects of newly planted hedges on
ground-beetle diversity (Coleoptera, Carabidae) in an agricultural land-
scape. Ecography 22: 87–97.
Fusser,M.S., S.C.Pster, M.H.Entling, and J.Schirmel. 2016. Effects of
landscape composition on carabids and slugs in herbaceous and woody
eld margins. Agric. Ecosyst. Environ. 226: 79–87.
Fusser,M.S., S.C.Pster, M.H.Entling, and J.Schirmel. 2017. Effects of eld
margin type and landscape composition on predatory carabids and slugs
in wheat elds. Agric. Ecosyst. Environ. 247: 182–188.
Gobbi,M., and D.Fontaneto. 2008. Biodiversity of ground beetles (Coleoptera:
Carabidae) in different habitats of the Italian Po lowland. Agric. Ecosyst.
Environ. 127: 273–276.
Gomiero,T., D.Pimentel, and M. G. Paoletti. 2011. Environmental impact
of different agricultural management practices: conventional vs. organic
agriculture. Crit. Rev. Plant Sci. 30: 95–124.
Holland,J.M. 2002. Carabid beetles: their ecology, survival and use in agro-
ecosystems, pp. 1–40. In J.M.Hooland (ed.), The agroecology of Carabid
beetles. Intercept Publication, Andover, MA.
Holland,J. M., and M. L. Luff. 2000. The effects of agricultural practices
on Carabidae in temperate agroecosystems. Integr. Pest Manage. Rev. 5:
109–129.
Howlett,S.A. 2012. Terrestrial slug problems: classical biological control and
beyond. CAB Rev. 7: 1–10
Kotze,D.J., P.Brandmayr, A.Casale, E.Dauffy-Richard, W.Dekoninck,
M. J. Koivula, G. L. Lövei, D. Mossakowski, J. Noordijk,
W.Paarmann, etal. 2011. Forty years of carabid beetle research in
Europe – from taxonomy, biology, ecology and population studies to
bioindication, habitat assessment and conservation. ZooKeys 100:
55–148.
Kromp, B. 1989. Carabid beetle communities (Carabidae, Coleoptera) in
biologically and conventionally farmed agroecosystems. Agric. Ecosyst.
Environ. 27: 241–251.
Langmaack,M., S.Land, and W.Büchs. 2001. Effects of different eld man-
agement systems on the carabid coenosis in oil seed rape with special
respect to ecology and nutritional status of predacious Poecilus cupreus
L.(Col., Carabidae). J. Appl. Entomol. 125: 313–320.
Langraf, V., K. Petrovičová, S. David, M. Ábelová, and J. Schlarmannová.
2017. Body volume in ground beetles (Carabidae) reects biotope disturb-
ance. Folia Oecol. 44: 114–120.
Legrand,A., C.Gaucherel, J.Baudry, and J.M.Meynard. 2011. Long-term
effects of organic, conventional, and integrated crop systems on Carabids.
Agron. Sust. Dev. 31: 515–524.
Lemic, D., M. Čačija, H. Virić Gašparić, Z. Drmić, R. Bažok, and
I.PajačŽivković. 2017. The ground beetle (Coleoptera: Carabidae) com-
munity in an intensively managed agricultural landscape. Appl. Ecol.
Environ. Res. J. 15: 661–674.
Luff,M. L. 1982. Population dynamics of Carabidae. Ann. Appl. Biol. 101:
164–170.
Magurran,A. E. 1988. Ecological diversity and its measurement. Princeton
University Press, Princeton, NJ.
Matalin,A. V. 1997. Specic features of life cycle of Pseudoophonus (s.str.)
rupes Deg. (Coleoptera, Carabidae) in the Southwestern Moldova, Izv.
Akad. Nauk. Ser. Biol. 4: 455–466.
Matalin,A.V. 2007. Typology of life cycles of ground beetles (Coleoptera,
Carabidae) from western Palaearctic. Zool. Zh. 86: 1196–1220.
Mazzoncini,M., S. Canali, M. Giovannetti, M.Castagnoli, F.Tittarelli,
D.Antichi, R.Nannelli, C.Cristani, and P.Barberi. 2010. Comparison
of organic and conventional stockless arable systems: a multidiscip-
linary approach to soil quality evaluation. Appl. Soil Ecol. 44: 124–132.
Mazzoncini,M., D.Antichi, N.Silvestri, G.Ciantelli, and C. Sgherri. 2015.
Organically vs conventionally grown winter wheat: effects on grain yield,
technological quality, and on phenolic composition and antioxidant prop-
erties of bran and rened our. Food Chem. 175: 445–451.
McKemey, A. R., D. M. Glen, and W. O. C. Symondson. 2004. How
does a carabid predator nd aggregations of slugs in the eld?
Electroantennograms and behavioural assays suggest chemical cues. Bull.
Entomol. Res. 94: 235–244.
Mendiburu,F.D. 2015. Agricolae: Statistical procedures for agricultural research.
R package version 1.2-3. http://CRAN.R- project.org/package=agricolae
Mori, A. S., T. Furukawal, and T.Sasaki. 2013. Response diversity deter-
mines the resilience of ecosystems to environmental change. Biol. Rev. 88:
349–364.
Naeem,S. 1998. Species redundancy and ecosystem reliability. Conserv. Biol.
12: 39–45.
Nazzi,F., M.G.Paoletti, and G.G.Lorenzoni. 1989. Invertebrate dynamics
of soybean agroecosystems encircled or not by hedgerows in Friuli, Italy.
First Data. Agric. Ecosyst. Environ. 27: 1–4.
Oberholzer, F., and T. Frank. 2003. Predation by the Carabid beetles
Pterostichus melanarius and Poecilus cupreus on slugs and slug eggs.
Biocontrol Sci. Techn. 13: 99–110.
Pesarini, C., and V.Monzini. 2010. Insetti della fauna italiana. Coleotteri
Carabidi I. Natura 100: 3–152.
Pesarini, C., and V.Monzini. 2011. Insetti della fauna italiana. Coleotteri
Carabidi II. Natura 101: 3–144.
Pizzolotto, R., A. Mazzei, T. Bonacci, S. Scalercio, N. Iannotta, and
P.Brandmayr. 2018. Ground beetles in Mediterranean olive agroecosys-
tems: their signicance and functional role as bioindicators (Coleoptera,
Carabidae). PLoS One 13: e0194551.
Porhajašová,J., A.Rakovská, J.Noskovič, M.Babošová, and T. Čeryová.
2014. Inuence of agroecosystems on biodiversity of Carabidae in the
nature reserve of Alúvium Žitavy in the southwestern part of the Slovak
Republic. Res. J.Agric. Sci. 46: 283–289.
Preacher,K.J. 2001. Calculation for the chi-square test: an interactive calcula-
tion tool for chi-square tests of goodness of t and independence. (http://
quantpsy.org) (accessed August 2019).
Purtauf,T., I.Roschewitz, J.Dauber, C.Thies, T.Tscharntke, and V.Wolters.
2005. Landscape context of organic and conventional farms: inuences on
carabid beetle diversity. Agric. Ecosyst. Environ. 108: 165–174.
Ranjha,M., and U.Irmler. 2014. Movement of carabids from grassy strips to
crop land in organic agriculture. J. Insect Conserv. 18: 457–467.
Rouabah, A., J. Villard, B. Amiaud, S. Plantureux, and F. Lasserre-Joulin.
2015. Response of Carabid beetles diversity and size distribution to the
10 Environmental Entomology, 2019, Vol. XX, No. XX
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
vegetation structure within differently managed eld margins. Agric.
Ecosyst. Environ. 200: 21–32.
Santini,L. 2000. Molluschi Gasteropodi. Cap.5, pp. 145–153. In B.Baccetti,
S. Barbagallo, L. Suss, and E. Trembaly (eds.), Manuale di Zoologia
Agraria. Antonio Delno Publication, Roma, Italy.
Sforzi,A., and L. Bartolozzi. 2001. Libro Rosso degli insetti della Toscana.
ARSIA, Agenzia Regionale per lo Sviluppo e l’Innovazione nel settore
Agricolo-forestale. Pub. EFFEEMME LITO, Firenze, Italy, 375 pp.
Shearin,A.F., S.C.Reberg-Horton, and E.R.Gallandt. 2007. Direct effects
of tillage on the activity density of ground beetle (Coleoptera: Carabidae)
weed seed predators. Environ. Entomol. 36: 1140–1146.
Shearin,A.F., S.C. Reberg-Horton, and E.R. Gallandt. 2008. Cover crop
effects on the activity-density of the weed seed predator Harpalus rupes
(Coleoptera: Carabidae). Weed Sci. 56: 442–450.
Snyder,E. M., H.D.Karsten, W. S.Curran, G. M. Malcolm, and J.Hyde.
2016. Green manure comparison between winter wheat and corn: weeds,
yields, and economics. Agron. J. 108: 1–11.
Sutter,L., M.Albrecht, and P.Jeanneret. 2017. Landscape greening and local
creation of wildower strips and hedgerows promote multiple ecosystem
services. J. Appl. Ecol. 55: 612–620.
Thomas, C. F. G., L. Parkinson, G. J. K. Grifths, A. F. Garcia, and
E. J. P. Marshall. 2001. Aggregation and temporal stability of carabid
beetle distributions in eld and hedgerow habitats. J. Appl. Ecol. 38:
100–116.
Tischler,W. 1949. Grundzüge der terrestrischen Tierökologie. Vieweg Verl.,
Braunschweig, Deutschland, Germany, 219 pp.
Tuf,I.H., P.Dedek, and M.Veselý. 2012. Does the diurnal activity pattern of
carabid beetles depend on season, ground temperature and habitat? Arch.
Biol. Sci. 64: 721–732.
Varchola,J.M., and J.P.Dunn. 2001. Inuence of hedgerow and grassy eld
borders on ground beetle (Coleoptera: Carabidae) activity in elds of corn.
Agric. Ecosyst. Environ. 83: 153–163.
Vernava, M. N., P. M. Phillips-Aalten, L. A. Hughes, H. Rowcliffe,
C.W.Wiltshire, and D.M.Glen. 2004. Inuences of preceding cover crops
onslug damage and biological control using Phasmarhabditis hermaphro-
dita. Ann. Appl. Biol. 145: 279–284.
VignaTaglianti,A. 2005. Checklist e corotipi di Carabidi della fauna italiana.
Appendice B, pp. 186–225. In P.Brandmayr, T. Zetto, and R.Pizzolotto
(eds.), Coleotteri Carabidi per la valutazione ambientale e la conservazi-
one della biodiversità. Manuale operative. APAT, Roma, Italy, 34.
Environmental Entomology, 2019, Vol. XX, No. XX 11
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvz119/5601195 by Università di Pisa user on 21 October 2019
