Archives of Agronomy and Soil Science

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Diversity and abundance of springtails (Hexapoda:

Collembola) in soil under 90-year potato
monoculture in relation to crop rotation

Jacek Piotr Twardowski, Micha Hurej & Iwona Gruss

To cite this article: Jacek Piotr Twardowski, Micha Hurej & Iwona Gruss (2016) Diversity and
abundance of springtails (Hexapoda: Collembola) in soil under 90-year potato monoculture
in relation to crop rotation, Archives of Agronomy and Soil Science, 62:8, 1158-1168, DOI:
10.1080/03650340.2015.1131270

To link to this article: http://dx.doi.org/10.1080/03650340.2015.1131270

Accepted author version posted online: 11

Dec 2015.
Published online: 09 Jan 2016.

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ARCHIVES OF AGRONOMY AND SOIL SCIENCE, 2016
VOL. 62, NO. 8, 11581168
http://dx.doi.org/10.1080/03650340.2015.1131270

Diversity and abundance of springtails (Hexapoda: Collembola)

in soil under 90-year potato monoculture in relation to crop
rotation
Jacek Piotr Twardowski, Micha Hurej and Iwona Gruss
Department of Plant Protection, Wroclaw University of Environmental and Life Science, Wroclaw, Poland

ABSTRACT ARTICLE HISTORY

The monoculture cropping system causes signicant changes within the Received 15 April 2015
soil ecosystem, which constitutes a habitat for soil-dwelling springtails. Accepted 9 December 2015
Focusing on the response of soil fauna to 90 years of potato cultivation KEYWORDS
in monoculture the study investigates the abundance and diversity of Collembola; crop rotation;
soil-dwelling springtails, considering changes in the soil environment in monoculture; potato; soil
relation to ve-crop rotation. Another point was the soil quality evalua- quality; springtails
tion using Collembola as bioindicators (QBS-c index). A long-term mono-
culture experiment was established in Poland in 1923 and has continued
uninterruptedly to the present time. Soil samples were taken over a
period of three years (20112013) to determine collembolan abundance
and composition, as well as physical and chemical soil properties.
The study demonstrated that there were greater numbers of
Collembola in the long-term monoculture of potatoes, especially before
planting time, compared to numbers in a ve-eld crop rotation. At the
same time apparently greater species diversity was found in potato
culture within crop rotation. The biological indicator of soil quality
based on the occurrence of springtails (QBS-c) has proved useful in
assessing changes in soil caused by agrotechnical activities. This index
indicated better biological soil quality in the ve-eld rotation system
compared to monoculture.

Introduction
Dierent agricultural practices have an important eect on soil biota, their activities and diversity
(Giller et al. 1997). There is also increasing interest in information on the impact of agricultural land
management on soil quality. The most destructive management practices such as tillage, applica-
tion of pesticides and mineral fertilizers signicantly aects communities of soil organisms as well
as their functional role in soil ecosystems (Frampton 1997; Rmbke et al. 2009; Twardowski 2010).
Modern agriculture is also characterized by long-term monoculture cropping system, which causes
negative changes in the soil structure, especially in soil compaction. This negatively aects soil
aggregate structure, which constitutes a habitat for soil organisms. The production of crops like
potatoes can substantially reduce soil quality and health. Monoculture increases some potato soil
pests like Globodera rostochiensis or soilborn plant pathogens like Fusarium spp. (Wharton et al.
2007; Tiilikkala 2008; Liu et al. 2014). Potato rotation is often characterized by low levels of organic
soil matter and consequently exhibits a poor soil physical condition. This is attributed mainly to
relatively low organic C input and generally sandy soil types associated with potato production,
which have a limited capability to retain organic C (Carter et al. 2003).

CONTACT Jacek Piotr Twardowski jacek.twardowski@up.wroc.pl

2016 Taylor & Francis
 ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1159

Springtails are one of the most numerous representatives of soil mesofauna (Neher &
Barbercheck 1999). Densities from about 100 to 670,000 individuals/m2 have been found in
dierent habitats, and as many as 60 dierent species may coexist within a few hectares
(Petersen & Luxton 1982). They typically constitute 2050% of the soil microarthropods, but in
some circumstances, e.g., at high elevations, they may have a dominant position (Crossley &
Coleman 1999; Jing et al. 2005). Euedaphic species of springtails live mostly in the surface soil
layer, down to 10 cm (Waikhom et al. 2006), while Ducarme et al. (2004) found that some species in
the temperate forest occur up to 1 m. Springtails respond relatively quickly to changes in soil
chemistry (Cassagne et al. 2003), pH (Ponge 2000), and microhabitat conditions like moisture (Xu
et al. 2012). The soil microclimate (mainly moisture and temperature) by favoring the activity of
mesofauna will aect the N mineralization of litter (Wang & Ruan 2011). Moreover, crop manage-
ment practices can lead to signicant changes in mesofauna species assemblages and diversity
(Frampton 1997; Alvarez et al. 2001; Carter & Noronha 2007). Generally, this group of arthropods is
benecial because they feed on decaying organic matter. Springtails enhance or inhibit dead
organic matter decomposition not as primary decomposers but mainly as microora regulators
of belowground food web (Seastedt 1984; Visser 1985). It is also known that pathogenic fungi are
Collembola food sources (Innocenti et al. 2011).
Soil-dwelling springtails are widespread and ecologically specialized, and therefore they are often
recommended as bioindicators of management-induced changes in soil quality and soil health
(Frampton 1997; Ponge et al. 2003). Soil quality can be evaluated by using a large number of
indicators (chemical, physical, biological) depending on scale and objective of the evaluation (Gardi
et al. 2002; Schloter et al. 2003). Based on Collembola species, the soil biological quality index (QBS-c)
was evaluated by some authors (Parisi 2001; Gardi et al. 2002; Parisi et al. 2005).
The study was conducted in a 90-year monoculture of potato, which is one of the oldest
monoculture experiments in Europe. Accordingly the following hypotheses were tested:

(1) The specic management in crop rotation promotes soil biota. The abundance, species
richness, and diversity of Collembola, as indicated by higher biological indices, are higher
in crop rotation than in monoculture.
(2) Soil quality is positively correlated with the number of Collembola species that are well-
adapted to soil habitats (Parisi 2001). In crop rotation occur more species with better
adaptations to live in soil, what indicate higher soil quality.
(3) Springtails can be used as good bioindicators of changes in soil environment. The use of
biological quality index based on Collembola species (QBS-c) and diversity indices can
provide a precise estimation of soil quality in agricultural ecosystems.

Thus, we investigated the abundance and diversity of soil-dwelling springtails, considering changes
in the soil environment as compared to ve-crop rotation.

Material and methods

Experimental site
The studied elds were located at the Experimental Station in Skierniewice, in the central part of
Poland, belonging to the faculty of Agriculture and Biology at Warsaw University of Life Sciences
(SGGW), (51.966135N, 20.163874E). A long-term static fertilization experiment was established in
Skierniewice in 1923 and has continued uninterruptedly to the present time. During the 90 years of
the experiment, farmyard manure used for organic fertilization has been applied at the same rates,
whereas nitrogen (N), phosphorus (P), and potassium (K) rates were changed according to existing
trends. Moreover, dierent potato cultivars have been used since the experiment was established. The
climate of the study area is transitional between maritime and continental. The annual mean rainfall of
1160 J. P. TWARDOWSKI ET AL.

Table 1. Agricultural treatments in monoculture and crop rotation.

Treatment Monoculture Crop rotation
Crop rotation Potatoes Potatoes by: barley, red clover,
winter wheat and winter rye
Cultivar Bila
Plant protection Herbicides: linuron, clomazone
Fungicides: uazinam, mancozeb, propamocarb, chlorothalonil
Fertilization CaO 1.6 t ha1 every 4 years, N (ammonium nitrate) 90 kg ha1,
P205 (superphosphate) 60 kg ha1 and K2O (potassium salt)
91 kg ha1 every year, 30 t ha1 of farmyard manure every 5 years
Other agricultural Ploughing to a depth of 25 cm
treatments Harrow ploughing to a depth of 15 cm
Potato planting
Ridging

three research years was 538 mm (the highest mean in July 97.4 and the lowest in February 27.5) and
annual mean temperature of +8.6C (the highest mean in July 19C and the lowest in January 1.47C).
The study was performed on a soil of the stagnic luvisol type, with clay and silt content in soil layers
(World Reference Base for Soil Resources 2006).
The agricultural practices performed during eld trials, in monoculture and crop rotation, are
provided in Table 1.
The experiment was established as a split plot with ve replicates in a randomized complete
block design. The monoculture plots were arranged in two blocks, and the crop rotation plots were
arranged in three blocks. Plants were grown in plots of 36 m2 (12 m 3 m). The distance between
the blocks was 3 m, and 1 m between the plots. Soil from individual plots was not mixed during
agricultural practices.

Sampling
Each year, soil samples were collected twice in spring within two weeks before potato planting (rst
half of April), and twice in autumn within two weeks after harvest (second half of September). The
choice of soil sampling terms was dictated by increased activity of mesofauna in spring and autumn,
which ensured representativeness for quantitative analyzes of faunistic material. To avoid potential
interference owing to plant growth, samples were not taken during the vegetation period.
Each time 25 soil samples were collected from each treatment (5 per plot, across the plot diagonal).
For sampling, a metal core sampler (5 cm diameter, 10 cm depth) with a cutting edge was used. Samples
were collected in plastic bags and then transported to the laboratory. Extraction of soil arthropods was
conducted in Tullgren funnels modied by Murphy (1956). Each sample was extracted over 24 hours. On
the basis of the conducted research, it was found that all springtails leave soil samples up to 24 h. After
extraction, springtails were counted under a stereomicroscope and preserved in 75% ethyl alcohol.
Individuals were prepared on permanent slides and identied to the species level under a light micro-
scope on the basis of existing keys (Zimdars & Dunger 2000; Fjellberg 2007; Hopkin 2007).

Physical and chemical soil properties

During the experiment, soil physicochemical properties were determined. Soil pH, since spring
2012, has been measured using an electronic pH meter (type Mettler Toledo model FE 20/FG2), in
water and KCl solution. Soil moisture and temperature were measured at each date at the depth of
5 cm by soil moisture and temperature sensor (type HH2) and gravimetric method. Soil particle size
distribution, organic matter, humus content, and mineral nitrogen in soil samples were determined
in the laboratory of the Chemical-Agricultural Station in Wrocaw, Poland.
In the remaining sampling dates, the soil temperature was almost the same in both agronomic
systems (Table 2). Soil moisture was slightly higher in crop rotation. The highest dierence was
 ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1161

Table 2. Soil physicochemical properties on sampling dates.

Treatment S* 2011 A 2011 S 2012 A 2012 S 2013 A 2013
Soil temperature (C)
Monoculture 7.7 15.2 7.9 13.2 17.8 10.1
Crop rotation 8.1 17.3 9.0 13.0 18.0 9.8
Soil moisture (%)
Monoculture 3.7 2.1 10.9 12.6 11.1 7.4
Crop rotation 3.9 2.4 12.5 14.6 11.9 11.5
pH (H2O)
Monoculture 6.3 7.7 6.3 7.1
Crop rotation 6.2 7.6 6.7 7.0
pH (KCl)
Monoculture 5.5 7.1 6.1 6.6
Crop rotation 5.7 6.2 6.7 6.6
*Sampling dates: S spring season, A autumn season.

found in autumn 2013, i.e., 11.5% in crop rotation and 7.4% in monoculture. Soils in both systems,
with the exception of spring 2012, showed pH around neutrality. The organic matter and humus
content were distinctly higher in crop rotation (0.77% and 1.32%) than in monoculture (0.38% and
0.66%, respectively). In addition, mineral nitrogen content was distinctly higher in crop rotation
(45.91 kg ha1) than in monoculture (30.06 kg ha1).
The studied soils were similar in particle size distribution. In both potato monoculture and crop
rotation, the clay fraction was in the range of 1112%, the granulometric class loamy sand (World
Reference Base for Soil Resources 2006).

Biological indices and data analysis

For each treatment, data on abundance of Collembola species were integrated to calculate the
ShannonWeaver (1948) and Simpson (1949) indices. The representation of the individuals in the
taxa (evenness) was evaluated through the Pielou (1966) index. Additionally, Srensens quantity
index (Magurran 2004), which determines species similarity between treatments, and the soil
biological quality index based on Collembola species (QBS-c) (Parisi 2001) were evaluated. This
QBS-c index classies Collembola species on the basis of morphological characteristics, assigning to
each species a dierent score, thereby dening the ecomorphological indices (EMIs) shown in Parisi
(2001). The QBS is calculated as the sum of EMI values in each soil. The underlying concept is that
soil quality is positively correlated with the number of Collembola species that are well adapted to
soil habitats. Abundance of Collembola was calculated separately for spring and autumn collection
using analysis of variance (ANOVA, p 0.05) in Statistica software, version 10.0.

Results
Springtails abundance and diversity
In 2011, in all samples collected in spring, an average of 2752 collembolans per m2 were calculated
in soil where the potato crop was grown in monoculture, while in the ve-eld rotation system
1610 individuals were found (Figure 1). In the samples collected in autumn of 2011, signicantly
more springtails were found in monoculture than in crop rotation (F ANOVA, F = 5.53, p = 0.023)
(1366/m2 and 407/m2, respectively). In 2012 and 2013, both in spring and in autumn, the
collembolan abundance was similar in both agronomic systems, although many more individuals
occurred in 2013. In spring of 2013, in monoculture, 2884 springtails per m2 were found, while in
2012 only 642 individuals. Similarly, in autumn of 2013 in crop rotation, 2812 collembolans per m2
were extracted from the soil, and only 968 in 2012.
In spring 2011, 7 Collembola species were identied in monoculture, 11 in crop rotation, and 6
species were common to both systems (Table 3). In monoculture, the most numerous species was
1162 J. P. TWARDOWSKI ET AL.

3500
Monoculture
3000
Crop rotation
2500
Individuals Nm-2

2000

1500 a*

1000
b
500

0
S** 2011 A 2011 S 2012 A 2012 S 2013 A 2013
Sampling dates

Figure 1. Springtails abundance in monoculture and crop rotation in 20112013.

*signicant dierence (ANOVA, p 0.05), **S spring, A autumn.

Table 3. Species composition and ecological parameters of springtails collected in spring 20112013.
2011 2012 2013
Crop Crop Crop
Monoculture rotation Monoculture rotation Monoculture rotation Total
Species N* D N D N D N D N D N D number
Mesaphorura macrochaeta (Rusek) 3 2.4 10 14.7 17 27.9 24 35.2 17 6.0 184 67.9 255
Desoria tigrina (Nicolet) 2 2.9 9 14.8 3 4.4 162 57.3 3 1.1 179
Hypogastrura manubrialis 90 71.4 14 20.6 9 14.8 11 16.2 38 13.4 15 5.5 177
(Tullberg)
Ceratophysella denticulata 1 1.5 43 15.1 16 5.8 60
(Bangall)
Bourletiella hortensis (Fitch) 8 6.3 1 1.5 19 31.1 6 8.8 8 2.8 8 3.0 50
Proisotoma minuta (Tullberg) 13 10.4 14 20.6 4 6.6 4 1.4 3 1.1 38
Brachystomella parvula (Scher) 3 2.4 16 23.5 1 1.6 1 1.5 1 0.4 12 4.4 34
Folsomia quadrioculata (Tullberg) 8 6.3 2 2.9 8 11.8 7 2.5 25
Parisotoma notabilis (Scher) 4 5.9 6 8.8 11 4.1 21
Desoria multisetis 1 0.8 4 5.9 5 1.8 10
(Carpenter&Phillips)
Protaphorura pannonica (Haybach) 1 1.5 1 1.5 1 0.4 4 1.5 7
Lepidocyrtus violaceus (Lubbock) 2 2.9 4 1.5 6
Isotoma viridis (Bourlet) 3 4.4 1 1.6 1 0.4 5
Sphaeridia pumilis (Krausbauer) 1 1.5 4 1.5 5
Isotomodes productus (Axelson) 1 1.5 2 0.7 1 0.4 4
Isotomurus fucicolus (Reuter) 1 1.6 1
Total 126 100 68 100 61 100 68 100 283 100 271 100 877
Species (N) 7 11 8 12 10 14 16
Common species 6 5 8
D 0.53 0.16 0.21 0.16 0.37 0.47
H 1.04 1.99 1.66 1.83 1.37 1.30
J 0.54 0.83 0.80 0.76 0.60 0.51
Sorensens quantity index
Monoculture 1 0.67 1 0.50 1 0.75
Crop rotation 0.67 1 0.50 1 0.75 1
*Ecological indices: N number of individuals or species, D dominance, H ShannonWeaver index, D Simpson index, J
Pielou index.

Hypogastrura manubrialis, which made up 71.4% of all identied springtails. In crop rotation three
species occurred in greater numbers: H. manubrialis, Proisotoma minuta, and Brachystomella
parvula, making up 20.6%, 20.6%, and 23.5% of all collembolans, respectively. Simpson and
 ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1163

Table 4. Species composition and ecological parameters of springtails collected in autumn 20112013.
2011 2012 2013
Crop Crop Crop
Monoculture rotation Monoculture rotation Monoculture rotation Total
Species N* D N D N D N D N D N D number
Mesaphorura macrochaeta (Rusek) 18 33.9 12 60.0 24 42.9 56 58.8 17 15.7 29 21.4 156
Desoria tigrina (Nicolet) 1 5.0 13 23.2 3 3.2 84 77.8 31 22.8 132
Hypogastrura manubrialis 3 5.7 2 10.0 3 5.4 14 14.7 2 1.9 59 43.4 83
(Tullberg)
Folsomia quadrioculata (Tullberg) 14 26.4 1 0.9 2 1.5 17
Ceratophysella denticulata 8 14.3 1 1.1 1 0.9 7 5.1 17
(Bangall)
Brachystomella parvula (Scher) 1 1.9 3 15.0 2 3.6 7 7.4 3 2.2 16
Desoria multisetis 2 3.8 1 1.8 9 9.4 12
(Carpenter&Phillips)
Parisotoma notabilis (Scher) 6 11.3 1 5.0 3 2.8 1 0.7 11
Proisotoma minuta (Tullberg) 8 15.1 1 1.1 9
Bourletiella hortensis (Fitch) 1 1.9 1 5.0 5 8.9 1 1.1 8
Protaphorura pannonica (Haybach) 2 2.1 1 0.7 3
Entomobrya spp. 3 2.2 3
Isotomodes productus (Axelson) 1 1.1 1
Total 53 100 20 100 56 100 95 100 108 100 136 100 468
Species (N) 8 6 7 10 6 10 13
Common species 5 7 6
D 0.21 0.37 0.26 0.38 0.66 0.28
H 1.69 1.24 1.54 1.34 0.64 1.52
(J) 0.73 0.69 0.67 0.58 0.39 0.69
Sorensens quantity index
Monoculture 1 0.77 1 0.82 1 0.71
Crop rotation 0.77 1 0.82 1 0.71 1
*Ecological indices: N number of individuals or species, D dominance, H ShannonWeaver index, D Simpson index, J
Pielou index.

ShannonWeaver indices suggested that springtails species diversity was higher in the crop
rotation system. In turn, the Pielou index showed higher evenness in this system than in mono-
culture. The value of the Srensen index was calculated as 0.67, which can be considered an
insignicant similarity.
In autumn of 2011, 8 and 6 springtail species were extracted from soil collected in monoculture
and in crop rotation, respectively (Table 4). Five species were common in both systems. In
monoculture after potato harvest, Mesaphorura macrochaeta was the dominant species, comprising
33.9% of all springtails. Folsomia quadrioculata also occurred in greater numbers, i.e., 26.4% of all
individuals. In crop rotation, the only numerous species was M. macrochaeta which made up 60%
of all identied collembolans in this treatment. Contrary to spring, in autumn the Simpson and
ShannonWeaver indices showed greater springtail diversity in the monoculture. The value of the
Pielou index was similar in both treatments (0.73 in monoculture and 0.69 in crop rotation). The
Srensen index (0.77) indicated high species similarity of both systems.
In 2012, in spring 8 (monoculture) and 12 (crop rotation) Collembola species were identied,
and 5 species were common (Table 3). In the monoculture, Bourlietiella hortensis and M.
macrochaeta were the most numerous. The rst species made up 31.1% and the second one
27.9% of all extracted individuals. In crop rotation, M. macrochaeta was also the dominant
species (35.2%), followed by H. manubrialis (16.2%). As in spring of the previous year, Simpson
and Shannon indices showed greater springtail diversity in crop rotation. Similarly, Pielou
indices calculated for monoculture (0.80) and for crop rotation (0.76) were almost the same.
The Srensen similarity index calculated between Collembola assemblages of both systems was
at a low level, only 0.50.
1164 J. P. TWARDOWSKI ET AL.

In autumn of 2012, once again more species were identied in plots with potato grown in ve-
eld rotation (10) (Table 4). In monoculture, seven species were identied, and also seven species
were common to both systems. In soil where potato was grown uninterruptedly to the present
time, M. macrochaeta was the dominant species and comprised 42.9% of all springtails. Desoria
tigrina also occurred in greater numbers (23.2%). In crop rotation, the only numerous species was
M. macrochaeta, which made up 58.8% of all identied collembolans in this treatment. Springtails
greater diversity in monoculture was found in autumn this year. The calculated value of the Pielou
index was 0.67 for monoculture and 0.58 for crop rotation. The Srensen similarity index (0.82)
indicated high species similarity of both systems.
In 2013, in spring, 10 species of springtails were extracted from soil collected in monoculture
and 14 species in crop rotation (Table 3). Eight species were common to both systems. It was the
greatest number of individuals and species identied in spring and in autumn in both treatments.
In monoculture, D. tigrina was the most numerous and constituted 57.3% of all collembolans.
Hypogastrura manubrialis and Ceratophysella denticulata also occurred in greater numbers, making
up 13.4% and 15.1% of springtails, respectively. In crop rotation, M. macrochaeta was clearly the
most abundant species (67.9% of all identied individuals). This spring, as in autumn of 2011 and
autumn of 2012, greater springtail diversity in monoculture was found. According to Pielou indices,
higher evenness was also found in this system than in crop rotation. The similarity between
Collembola assemblages of both systems was calculated on 0.75 level.
In autumn of 2013, only 6 species were collected in monoculture, whereas in crop rotation 10
species were collected (Table 4). All six species which occurred in soil samples from monoculture
were also found in samples from crop rotation. Desoria tigrina, making up 77.8% of all collembolans
in monoculture, was clearly the dominant species. In crop rotation, three species were most
abundant: H. manubrialis (43.4%) followed by D. tigrina (22.8%) and then M. macrochaeta
(21.4%). Simpson and ShannonWeaver indices showed greater springtail diversity in crop rotation
in autumn 2013. Pielou indices also showed higher evenness in this system. The calculated
similarity level between springtail assemblages in the investigated soils was 0.71.

Soil quality according to QBS-c index

The EMI values of springtail species recorded in soil samples in our trials are presented in Table 5.
The highest EMI values were assigned to species best adapted to the soil habitat, such as M.
macrochaeta or Protaphorura pannonica and Isotomodes productus (euedaphic species). The lowest

Table 5. EMI values of Collembola species identied in soil samples.

Species EMI
Mesaphorura macrochaeta 37
Protaphorura pannonica 33
Isotomodes productus 25
Brachystomella parvula 21
Ceratophysella denticulata 17
Hypogastrura manubrialis 17
Sinella curviseta 15
Folsomia quadrioculata 13
Parisotoma notabilis 13
Desoria multisetis 10
Desoria tigrina 10
Isotoma viridis 10
Proisotoma minuta 10
Bourletiella hortensis 8
Sphaeridia pumilis 8
Entomobrya spp. 1
Isotomurus fucicolus 1
Lepidocyrtus violaceus 1
 ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1165

Table 6. Soil quality index based on the evaluation of springtails (QBS-c).

Monoculture Crop rotation
Spring 2011 116 189
Autumn 2011 129 129
Spring 2012 114 196
Autumn 2012 120 188
Spring 2013 191 220
Autumn 2013 94 162
Mean 127.3 180.7

EMI values were assigned to epigeic species such as Isotomurus fucicolus, Lepidocyrtus violaceus,
and Entomobrya spp. Most species identied in soil samples were hemiedaphic with the medium
EMI values, such as H. manubrialis, D. multisetis, or P. minuta.
At each sampling date, except for autumn of 2011, the biological soil quality index specic
for Collembola (QBS-c) was higher in the treatment in which potato was grown in rotation as
compared to monoculture (Table 6). The highest value was calculated in crop rotation in
spring 2012 (220), and the lowest value in monoculture in autumn of 2013 (94). The mean
QBS-c index for six sampling dates is much higher in crop rotation (180.7) than in mono-
culture: (127.3).

Discussion
Agricultural intensication strongly aects ecosystem diversity, including the soil ecosystem. Most
important factors include plant selection and their cultivation in monoculture, tillage system, and
application of pesticides or mineral fertilizers. In general, these practices tend to reduce soil
biodiversity including springtails (Giller et al. 1997; Graenitz & Bauer 2000; Twardowski 2010;
Kalia & Gosal 2011). Cultivation in monoculture deteriorates physicochemical soil properties and
leads to numerous negative consequences, such as pest outbreaks, accumulation of pathogens and
changes in the abundance and activity of soil-dwelling springtails (Mussury & Scalon 2002). Crop
rotation, on the other hand, increases organic matter content and improves the soil structure
(Rychcik et al. 2006).
Intensively managed monocultures are characterized by Collembola communities with low
species richness and abundance (Winkler & Traser 2012). In the studied arable soils, a maximum
of 14 collembolan species (crop rotation, spring 2013) and 2884 individuals per m2 (monocul-
ture, spring 2013) were found on one sampling date. Low densities and species richness of
Collembola in arable soils are reported from dierent countries (Rusek 1998; Kanal 2004; Muturi
et al. 2009; Flores-Pardav et al. 2011). This is usually the result of intensive farming. We
suppose that the low occurrence of Collembola could be the eect of relatively low soil
moisture in sampling dates (even 2.1%). All the springtails identied in the experiment belong
to cosmopolitan species. Many of them (M. macrocheta, Isotoma viridis, P. minuta, Parisotoma
notabilis, I. productus, F. quadrioculata, Sphaeridia pumilis) were also found in other agroecosys-
tems in soils with similar conditions (Twardowski 2010). The most abundant species in both
systems was M. macrochaeta, which can be considered as species occurring in a large number in
intensively managed soils.
In contrast to the rst hypothesis, the abundance of springtails was similar in both studied
systems. Contrary to our results, in similar experiment conducted in winter rye crop we found more
springtails in winter rye cultivated in ve-crop rotation than in long-term monoculture (Gruss &
Twardowski 2012). In turn, Kanal (2004) indicates that the long-term crops in monoculture can
promote specic assemblages of springtails, showing adaptations to local soil conditions. Probably
in the present study, the monoculture system might have a more direct eect on the quantity of
Collembola owing to longer adaptation time with a particular crop than is possible in the case of
1166 J. P. TWARDOWSKI ET AL.

crop rotation. On the other hand, as we expected, the species richness of Collembola, as well as
their diversity (Simpson and ShannonWeaver indices) and evenness were higher in crop rotation
(in ve of the six sampling dates more species were found in crop rotation). This was probably
aected by distinctly higher organic matter and humus content in that system. Similar to our
studies, many authors indicate that the abundance of soil mesofauna is higher in places with
relatively high organic matter and humus content (Kovac & Miklisova 1997; Mema Devi et al. 2011).
Battigelli et al. (2004) explained that organic matter supplies nutrients and improves soil porosity,
which creates a suitable habitat for soil mesofauna.
Numerous occurrences of euedaphic forms of springtails in a given habitat can indicate better
biological quality of the soil (Parisi 2001). In the research of Kanal (2004) conducted within a potato
ecosystem, it was found that euedaphic forms dominated in the soil of arable land, while the most
stable environment for the development of the Collembola occurs in the deeper layers of the soil.
In the present research, this statement was conrmed using the QBS-c index. This index was not
often used in a similar evaluation. Up to now, it was more often used in the assessment of soil
quality in urban areas (Santofuro et al. 2012) or forest ecosystems (Ballabio et al. 2013). Using the
QBS-c index, it was found that springtails seem to be good indicators of soil quality in agroeco-
systems. The highest QBS-c index was calculated when the well-adapted species were numerous in
collected samples. In degraded soil environments, springtail species diversity decreases, so the high
value of the index QBS-c indicates the good quality of the soil (Jacomini et al. 2000). Gardi et al.
(2002) reported that the value of the indicator QBS-c in agricultural soils is usually less than 100,
and meadow or forest reach higher values. In the present experiment in potato, the average eld
value of QBS-c exceeded 100. As we hypothesized, in crop rotation there were more species well
adapted to soil habitats. The potato QBS-c index indicated that the quality of the soil in a ve-eld
crop rotation was obtained 180.7 and 127.3 for monoculture.
The results of the present study indicate that long-term cultivation of potato in monoculture
(90 years) considerably aects soil-dwelling springtails. It can be assumed that changes which
occurred in too long cultivation of one crop species in the same place (including varieties) are
permanent. Dierences between the parameters describing the physicochemical conditions of
the soil consequently signicantly aect the organisms discussed. It should be noted that the
obtained results are not conclusive and cannot be easily evaluated in monoculture cultivation as
the only negative factor. In the case of potato cultivation in monoculture, springtails often
increased their number as compared to ve-crop rotation stands. Critical assessment of crops in
monoculture is not consistent with the fact that on many farms it produces better economic
results.

Conclusion
The study demonstrated that there were a large number of Collembola in the long-term mono-
culture of potatoes, especially before planting time, as compared to a ve-eld crop rotation.
However, at the same time clearly greater species diversity was found in potato cultivation in crop
rotation. As we hypothesized, the biological indicator of soil quality assessment based on the
occurrence of springtails (QBS-c) was useful in assessing changes in soil caused by agrotechnical
activities. It was found that the higher quality of potato cultivation of the soil was characterized by
the position of a ve-eld rotation compared to monoculture.

Acknowledgements
We are greatly indebted to the sta of the Experimental Research Station in Skierniewice, belonging to faculty of
Agriculture and Biology, Warsaw University of Life Sciences, for their help in eld preparation.
 ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1167

Disclosure statement
No potential conict of interest was reported by the authors.

Funding
This work was supported by the Polish Ministry of Science and Higher Education [grant number NN310303139].

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