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Archives of Agronomy and Soil Science ISSN: 0365-0340 (Print) 1476-3567 (Online) Journal homepage:
Archives of Agronomy and Soil Science ISSN: 0365-0340 (Print) 1476-3567 (Online) Journal homepage:

Archives of Agronomy and Soil Science

ISSN: 0365-0340 (Print) 1476-3567 (Online) Journal homepage: http://www.tandfonline.com/loi/gags20

Diversity and abundance of springtails (Hexapoda:

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

Jacek Piotr Twardowski, Michał Hurej & Iwona Gruss

To cite this article: Jacek Piotr Twardowski, Michał 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:

Accepted author version posted online: 11 Dec 2015. Published online: 09 Jan 2016.

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, 1158 1168

http://dx.doi.org/10.1080/03650340.2015.1131270

ARCHIVES OF AGRONOMY AND SOIL SCIENCE, 2016 VOL. 62, NO. 8, 1158 – 1168 http://dx.doi.org/10.1080/03650340.2015.1131270
ARCHIVES OF AGRONOMY AND SOIL SCIENCE, 2016 VOL. 62, NO. 8, 1158 – 1168 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, Michał Hurej and Iwona Gruss

Department of Plant Protection, Wroclaw University of Environmental and Life Science, Wroclaw, Poland

ABSTRACT

The monoculture cropping system causes signi cant changes within the soil ecosystem, which constitutes a habitat for soil-dwelling springtails. Focusing on the response of soil fauna to 90 years of potato cultivation in monoculture the study investigates the abundance and diversity of soil-dwelling springtails, considering changes in the soil environment in relation to ve-crop rotation. Another point was the soil quality evalua- 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 (2011 2013) 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.

ARTICLE HISTORY

Received 15 April 2015 Accepted 9 December 2015

KEYWORDS

Collembola; crop rotation; monoculture; potato; soil quality; springtails

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 a ects communities of soil organisms as well as their functional role in soil ecosystems (Frampton 1997 ; Römbke 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 a ects 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

© 2016 Taylor & Francis

C (Carter et al. 2003 ). CONTACT Jacek Piotr Twardowski © 2016 Taylor & Francis jacek.twardowski@up.wroc.pl

jacek.twardowski@up.wroc.pl

ARCHIVES OF AGRONOMY AND SOIL SCIENCE

ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1159 Springtails are one of the most numerous representatives of

1159

Springtails are one of the most numerous representatives of soil mesofauna (Neher & Barbercheck 1999 ). Densities from about 100 to 670,000 individuals/m 2 have been found in dierent habitats, and as many as 60 di erent 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 signi cant 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 speci c 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), (51.966135ʹN, 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

1160 J. P. TWARDOWSKI ET AL. Table 1. Agricultural treatments in monoculture and crop rotation. Treatment

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 Herbicides: linuron, clomazone Fungicides: uazinam, mancozeb, propamocarb, chlorothalonil CaO 1.6 t ha 1 every 4 years, N (ammonium nitrate) 90 kg ha 1 , P 2 0 5 (superphosphate) 60 kg ha 1 and K 2 O (potassium salt) 91 kg ha 1 every year, 30 t ha 1 of farmyard manure every 5 years Ploughing to a depth of 25 cm Harrow ploughing to a depth of 15 cm Potato planting Ridging

Plant protection

Fertilization

Other agricultural

treatments

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 +8.6ºC (the highest mean in July 19ºC and the lowest in January 1.47ºC). 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 m 2 (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 Wroc ław, 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 di erence was

Table 2. Soil physicochemical properties on sampling dates.

ARCHIVES OF AGRONOMY AND SOIL SCIENCE

on sampling dates. ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1161 Treatment S * 2011 A 2011

1161

Treatment

S * 2011

A 2011

S 2012

A 2012

S 2013

A 2013

Soil temperature (ºC) Monoculture Crop rotation Soil moisture (%) Monoculture Crop rotation pH (H 2 O) Monoculture Crop rotation pH (KCl) Monoculture Crop rotation

7.7

15.2

7.9

13.2

17.8

10.1

8.1

17.3

9.0

13.0

18.0

9.8

3.7

2.1

10.9

12.6

11.1

7.4

3.9

2.4

12.5

14.6

11.9

11.5

6.3

7.7

6.3

7.1

6.2

7.6

6.7

7.0

5.5

7.1

6.1

6.6

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 ha 1 ) than in monoculture (30.06 kg ha 1 ). The studied soils were similar in particle size distribution. In both potato monoculture and crop rotation, the clay fraction was in the range of 11 12%, 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, Sørensen s 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 di erent 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

Springtailsabundance and diversity

In 2011, in all samples collected in spring, an average of 2752 collembolans per m 2 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/m 2 and 407/m 2 , 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 m 2 were found, while in 2012 only 642 individuals. Similarly, in autumn of 2013 in crop rotation, 2812 collembolans per m 2 were extracted from the soil, and only 968 in 2012. In spring 2011, 7 Collembola species were identi ed 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 2000 a* 1500
1162
J. P. TWARDOWSKI ET AL.
3500
Monoculture
3000
Crop rotation
2500
2000
a*
1500
1000
b
500
0
Individuals Nm-2

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 di erence (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

ND

N

D

ND

N

D

ND

number

Mesaphorura macrochaeta (Rusek) Desoria tigrina (Nicolet) Hypogastrura manubrialis (Tullberg) Ceratophysella denticulata (Bangall) Bourletiella hortensis (Fitch) Proisotoma minuta (Tullberg) Brachystomella parvula (Schäer) Folsomia quadrioculata (Tullberg) Parisotoma notabilis (Schä er) Desoria multisetis (Carpenter&Phillips) Protaphorura pannonica (Haybach) Lepidocyrtus violaceus (Lubbock) Isotoma viridis (Bourlet) Sphaeridia pumilis (Krausbauer) Isotomodes productus (Axelson) Isotomurus fucicolus (Reuter) Total Species ( N ) Common species D HJ Sorensens quantity index Monoculture Crop rotation

3

2.4

10 14.7

17

27.9

24 35.2

17

6.0

184 67.9

255

 

2

2.9

9

14.8

3

4.4

162

57.3

3

1.1

179

90

71.4

14 20.6

9

14.8

11 16.2

38

13.4

15

5.5

177

 

1

1.5

43

15.1

16

5.8

60

8

6.3

1

1.5

19

31.1

6

8.8

8

2.8

8

3.0

50

13

10.4

14 20.6

4

6.6

4

1.4

3

1.1

38

3

2.4

16 23.5

1

1.6

1

1.5

1

0.4

12

4.4

34

8

6.3

2

2.9

8 11.8

7

2.5

25

 

4

5.9

6

8.8

11

4.1

21

1

0.8

4

5.9

5

1.8

10

 

1

1.5

1

1.5

1

0.4

4

1.5

7

 

2

2.9

4

1.5

6

 

3

4.4

1

1.6

1

0.4

5

 

1

1.5

4

1.5

5

1

1.5

2

0.7

1

0.4

4

 

1

1.6

1

126

100

68 100

61

100

68 100

283

100

271 100

877

7

11

8

12

10

14

16

6

5

8

0.53

0.16

0.21

0.16

0.37

0.47

1.04

1.99

1.66

1.83

1.37

1.30

0.54

0.83

0.80

0.76

0.60

0.51

1

0.67

1

0.50

1

0.75

0.67

1

0.50

1

0.75

1

*Ecological indices: N number of individuals or species, D dominance, H’– Shannon Weaver 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

ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1163 Table 4. Species composition and ecological parameters of springtails

1163

Table 4. Species composition and ecological parameters of springtails collected in autumn 20112013.

2011

Crop

2012

Crop

2013

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 Desoria tigrina (Nicolet) Hypogastrura manubrialis (Tullberg)

3

33.9

12 60.0

24

42.9

56 58.8

17

15.7

29 21.4

156

1

5.0

13

23.2

3

3.2

84

77.8

31 22.8

132

5.7

2 10.0

3

5.4

14 14.7

2

1.9

59 43.4

83

Folsomia quadrioculata (Tullberg) Ceratophysella denticulata (Bangall) Brachystomella parvula (Schäer) Desoria multisetis (Carpenter&Phillips) Parisotoma notabilis (Schä er) Proisotoma minuta (Tullberg) Bourletiella hortensis (Fitch) Protaphorura pannonica (Haybach) Entomobrya spp. Isotomodes productus (Axelson) Total Species ( N ) Common species D H( J ) Sorensens quantity index Monoculture Crop rotation

14

26.4

1

0.9

2

1.5

17

 

8

14.3

1

1.1

1

0.9

7

5.1

17

1

1.9

3 15.0

2

3.6

7

7.4

3

2.2

16

2

3.8

1

1.8

9

9.4

12

6

11.3

1

5.0

3

2.8

1

0.7

11

8

15.1

1

1.1

9

1

1.9

1

5.0

5

8.9

1

1.1

8

 

2

2.1

1

0.7

3

 

3

2.2

3

 

1

1.1

1

53

100

20 100

56

100

95 100

108

100

136 100

468

8

6

7

10

6

10

13

5

7

6

0.21

0.37

0.26

0.38

0.66

0.28

1.69

1.24

1.54

1.34

0.64

1.52

0.73

0.69

0.67

0.58

0.39

0.69

1

0.77

1

0.82

1

0.71

0.77

1

0.82

1

0.71

1

*Ecological indices: N number of individuals or species, D dominance, H’– Shannon Weaver index, D’– Simpson index, J ’ – Pielou index.

ShannonWeaver indices suggested that springtailsspecies 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 Sørensen 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 Sørensen index (0.77) indicated high species similarity of both systems. In 2012, in spring 8 (monoculture) and 12 (crop rotation) Collembola species were identi ed, 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 Sørensen similarity index calculated betw een Collembola assemblages of both systems was at a low level, only 0.50.

1164

1164 J. P. TWARDOWSKI ET AL. In autumn of 2012, once again more species were identi

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 identi ed, 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 identi ed 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 Sørensen 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 Shannon Weaver 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 Protaphorura pannonica Isotomodes productus Brachystomella parvula Ceratophysella denticulata Hypogastrura manubrialis Sinella curviseta Folsomia quadrioculata Parisotoma notabilis Desoria multisetis Desoria tigrina Isotoma viridis Proisotoma minuta Bourletiella hortensis Sphaeridia pumilis Entomobrya spp. Isotomurus fucicolus Lepidocyrtus violaceus

37

33

25

21

17

17

15

13

13

10

10

10

10

8

8

1

1

1

ARCHIVES OF AGRONOMY AND SOIL SCIENCE

ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1165 Table 6. Soil quality index based on the evaluation

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 20 11, the biological soil quality index speci c for Collembola (QBS-c) was higher in the trea tment 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 hig her in crop rotation (180.7) than in mono- culture: (127.3).

Discussion

Agricultural intensi cation strongly a ects 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 m 2 (monocul- ture, spring 2013) were found on one sampling date. Low densities and species richness of Collembola in arable soils are reported from di erent countries (Rusek 1998 ; Kanal 2004 ; Muturi et al. 2009 ; Flores-Pardav ė et al. 2011 ). This is usually the result of intensive farming. We suppose that the low occurrence of Collembola could be the e ect of relatively low soil moisture in sampling dates (even 2.1%). All the springtails identi ed 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 speci c assemblages of springtails, showing adaptations to local soil conditions. Probably in the present study, the monoculture system might have a more direct e ect on the quantity of Collembola owing to longer adaptation time with a particular crop than is possible in the case of

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1166 J. P. TWARDOWSKI ET AL. crop rotation. On the other hand, as we expected, the

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 a ects 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. Di erences between the parameters describing the physicochemical conditions of the soil consequently signi cantly a ect 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. Cr itical 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

ARCHIVES OF AGRONOMY AND SOIL SCIENCE Disclosure statement No potential con fl ict of interest was

Disclosure statement

No potential con ict of interest was reported by the authors.

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Funding

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

References

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