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Article

Comparison of the Effect of Perennial Energy Crops and Arable Crops on Earthworm Populations

by
Beata Feledyn-Szewczyk
*,
Paweł Radzikowski
,
Jarosław Stalenga
and
Mariusz Matyka
Department of Systems and Economics of Crop Production, Institute of Soil Science and Plant Cultivation—State Research Institute, Czartoryskich 8 Str., 24-100 Puławy, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2019, 9(11), 675; https://doi.org/10.3390/agronomy9110675
Submission received: 1 October 2019 / Revised: 18 October 2019 / Accepted: 22 October 2019 / Published: 24 October 2019
(This article belongs to the Special Issue Impact of Agricultural Practices on Biodiversity of Soil Invertebrates)
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Abstract

:
The purpose of the study was to compare earthworm communities under winter wheat in different crop production systems on arable land—organic (ORG), integrated (INT), conventional (CON), monoculture (MON)—and under perennial crops cultivated for energy purposes—willow (WIL), Virginia mallow (VIR), and miscanthus (MIS). Earthworm abundance, biomass, and species composition were assessed each spring and autumn in the years 2014–2016 using the method of soil blocks. The mean species number of earthworms was ordered in the following way: ORG > VIR > WIL > CON > INT > MIS > MON. Mean abundance of earthworms decreased in the following order: ORG > WIL > CON > VIR > INT > MIS > MON. There were significantly more species under winter wheat cultivated organically than under the integrated system (p = 0.045), miscanthus (p = 0.039), and wheat monoculture (p = 0.002). Earthworm abundance was significantly higher in the organic system compared to wheat monoculture (p = 0.001) and to miscanthus (p = 0.008). Among the tested energy crops, Virginia mallow created the best habitat for species richness and biomass due to the high amount of crop residues suitable for earthworms and was similar to the organic system. Differences in the composition of earthworm species in the soil under the compared agricultural systems were proven. Energy crops, except miscanthus, have been found to increase earthworm diversity, as they are good crops for landscape diversification.

1. Introduction

Earthworms constitute the largest component of animal biomass in the soil, and they are termed “soil engineers” [1] or even “ecosystem engineers” [2]. The diversity and abundance of earthworms are an important criterion of soil fertility [3]. Earthworms play a major role in the processes of decomposition of plant and animal organic residues, soil humus formation, creation of a crumbly soil structure, water regulation, pathogen and pest control, degradation of pollutants, as well as nitrogen binding [2,4]. Earthworms provide many ecosystem services, such as maintenance of proper soil structure, soil humus formation, nutrient cycling, erosion control, and biological crop protection [5].
Activity of earthworms and formation of burrows improve the aeration and water infiltration and therefore reduce surface runoff [6]. There are many mineral and organic ingredients in earthworm excrements that are beneficial for the growth and development of plants. These fractions are well mixed in worm casts, and the nutrients are present in a readily available form [1,5]. Soil passing through the digestive system of earthworms is enriched with beneficial microorganisms binding free nitrogen and activating phosphorus, which become available to plants. Both excreta and secretions (metabolic water and mucus) of earthworms contain plant growth stimulators (auxin, gibberellin, and cytokine), affecting the quality and quantity of the crop yield [7]. By pulling fallen leaves into the soil, foliar pathogens and pests are biologically degraded. Earthworms distribute insect-killing nematodes (Steinernema sp.) and fungi (Beauveria bassiana) in the soil, thus contributing to better natural regulation of soil-borne pests. Earthworms ingest organic residues of different C:N ratios, convert them to a lower C:N ratio, and finally contribute to carbon sequestration [5]. A rich earthworm fauna is a key in maintaining and safeguarding soil health and in fostering many essential ecosystem functions of soil.
Agricultural practices, such as tillage, crop rotation, cultivation of catch crops (defined here as additional fast-growing crops grown between successive plantings of main crops), the use of mineral fertilizers, and pesticides all have significant impacts on wild flora and fauna, including soil organisms [8,9,10]. The sensitivity of earthworms to unfavourable changes in agrocenosis makes them a good indicator of the ecological footprint of agricultural systems [11]. According to Pfiffner [5], the following measures are prerequisites for the flourishing of earthworms in agricultural soils: provision of sufficient food, abstinence from the use of pesticides harmful to earthworms, application of soil-conservation methods such as reduced tillage and no-till, avoidance of soil compaction and promotion of well-structured and aerated soils, appropriate fertilization, and balanced humus management within the crop rotation. Different farming systems can support or reduce biodiversity and soil settlement by earthworms. High-input conventional agriculture reduces the biodiversity of earthworms, whereas conservation and organic agriculture benefit this group of organisms [12,13,14].
Cultivation of perennial crops for energy purposes is still a new agricultural system so little scientific evidence appears to be available on the effects of these types of crops on the environment, including on earthworm populations [15,16]. The positive effect of energy crops on biodiversity is connected with the lower agrochemical input as compared to the intensive production used in annual crops [15,17,18,19]. Due to the unknown impact of many plant species used for energy purposes on the environment and biodiversity, there should be wide-ranging and long-term ecological monitoring conducted for these crops [19,20]. According to Verdade et al. [21], biodiversity monitoring programs are needed to help the decision-making process concerning the conflict between the expansion of energy crops and the conservation of biodiversity. These programs should take into account comparisons with neighbouring agricultural crops [22,23]. Such a comparison has been done in this current study.
Our hypothesis was that the cultivation of certain species of perennial energy crops stimulate earthworm diversity and abundance more than farming systems on arable land.
On this basis, the aim of the present research was to compare the impact of various agricultural systems on arable land (organic, integrated, conventional, and winter wheat monoculture) and the impact of cultivation of perennial energy crops (miscanthus, Virginia mallow, and willow) on earthworm diversity, abundance, and biomass under the conditions pertaining in Eastern Poland (Central Europe).

2. Materials and Methods

2.1. Site Description and Experimental Design

The assessment of earthworms was carried out as part of a long-term field experiment (1994–until now) with four crop production systems: organic (ORG), integrated (INT), conventional (CON), and monoculture-conventional (MON) (Table 1). Experimental plantations of perennial energy crops (2008–until now)—miscanthus (Miscanthus sp.) (MIS), Virginia mallow (Sida hermaphrodita) (VIR), and willow (Salix viminalis) (WIL)—have been established 70–100 m away from the crop production systems on the arable land described above. The experimental sites are located at the Agricultural Research Station of the Institute of Soil Science and Plant Cultivation—State Research Institute (IUNG-PIB) in Osiny (Poland, Lublin voivodeship, N: 51°28′, E: 22°30′) on Haplic Luvisol soil [24] with a texture of loamy sand. The chemical properties of the soil in the different farming systems are presented in Table 2. Average annual total precipitation of the experimental site was 586 mm with a mean air temperature of 7.5 °C (data for the years 1950–2013).
The tested farming systems on arable land were characterised by different crop rotations and agricultural management (Table 1). In the organic system, no synthetic pesticides and natural phosphorus (P) and potassium (K) fertilizers such as crude potassium salt or kainite as well as compost, applied once in a crop rotation, under potato (30 t ha−1) were applied. High-input conventional systems included two variants: (1) 3-field crop rotation: winter oilseed rape, winter wheat, and spring wheat and (2) winter wheat monoculture. In both objects, crops were cultivated intensively, i.e., with high rates of synthetic mineral fertilizers and pesticides (Table 1). In the integrated system balanced mineral and organic fertilization (about 20–30% lower than in conventional system), adaptation to the crop requirements and soil fertility were used. Soil tillage was similar in all crop production systems; in general, it was a traditional plough system. Before sowing of winter crops, a four-furrow reversible plough was used at depths of 15–20 cm. Before sowing of spring crops, winter ploughing was carried out at a depth of minimum 20 cm. After late crops such as maize or potato or after cultivation of a catch crop, winter ploughing was done usually in the second half of November. For other crops harvested in July/August, winter ploughing was performed at the end of September. Before sowing, a compact seedbed cultivator was usually used. Number and time of ploughing treatments in particular systems depended on the crop rotation structure.
Crop protection consisted of nonchemical (mechanical) measures, and only a limited number of herbicides and other plant protection products were applied based on harmfulness thresholds. Most herbicides used were applied on crops, and only a few based on glyphosate were sprayed on stubble and incorporated into soil.
The analyses were carried out in the soil under winter wheat cv. Jantarka, which grew in all of these crop production systems. The area of each field was 1 ha so it was possible to manage them using real agricultural practices. In energy crops, no chemical crop protection measures have been performed during the study period. The area of the energy crop fields was from 200 m2 (miscanthus and Virginia mallow) to 500 m2 (willow).

2.2. Earthworm Collection

Earthworms were collected in the years 2014–2016, according to the method of soil blocks [25]. Samples were taken twice in each season: in spring (April) and in autumn (October), when soil temperature and moisture are usually suitable for earthworm activity. Soil blocks 25 cm × 25 cm × 25 cm (0.0625 m2 of arable soil layer) were dug out of each field in 5 replications. The blocks were separated by at least 5 m from each other and 5 m away from the field margin to avoid the edge effect. Soil blocks were placed on a sheet on which the earthworms were caught and kept in collecting containers. The earthworms were transported in cool boxes to the laboratory, where they were washed, weighed, and preserved in 4% formalin for further investigations. In later terms, earthworms were classified into species according to an identification guide [26]. The species was recognized on the basis of morphological features. The structure of the mouth, distribution of bristles, number of segments, structure and location of the reproductive organs, and the location of secretory holes were thoroughly analyzed. Due to longer storage in the formalin solution, the colour of individuals was not taken into account. Both mature and young forms were considered, but only adult individuals were defined to the species [5]. Earthworm species richness, their abundance, and biomass (fresh weight) were taken into account as biodiversity indicators. Earthworm density and biomass were calculated per 1 m2. For each investigated agricultural system, the results from all terms of collection were presented (3 years × 2 terms × 5 replications = 30 samples for each studied field).

2.3. Statistical Analyses

Because this trial was without replication, we chose to consider each sample point as a replicate, though this approach could have induced some bias because of pseudoreplications. We are, however, quite confident that, for several reasons, our sampling design allowed us to use this approach: (i) sample points within a field were far enough away from each other (20 m) to ensure replicate independence, and (ii) the possibility that the sample fields were affected by confounding factors due to limited randomization cannot be excluded but was limited as the trial was evenly affected by the same management before the trial setup, topographic and pedologic gradients were controlled, and a preliminary assessment of the trial spatial heterogeneity was found to be very low within the block soil heterogeneity. This methodological approach has been used earlier by Henneron et al. [14]. There are examples of field trials that are not replicated, for example, one of the oldest long-term experiments established in 1843 Rothamsted (UK) [27], but, with the help of specific statistical methods, permits reliable comparisons. Lack of replications is due to different reasons, but usually, it is caused by physical constraints such as land availability or plot size. Sometimes financial or social limitations are also important [28].
In order to check the normality of the distributions, the Shapiro–Wilk test was used. The obtained data sets were characterized by a non-normal distribution; therefore, the nonparametric Kruskal–Wallis rank test was used to assess the significance of differences in the examined features at the significance level p ≤ 0.05. Statistical analyses were performed using Statistica 10 software (Stat. Soft. Inc., Tulsa, OK, USA).
In order to group the earthworm communities, a cumulative hierarchical classification was done using MVSP 3.1. software, Kovach Computing Services, Anglesey, Wales [29]. The quantitative Sorensen’s similarity index (Percent Similarity) was used to classify similarities between earthworms under different farming systems and types of energy crops [30].
In order to classify the samples based on earthworm species composition and species based on their participation in the samples, ordination techniques were used [31]. As first, Detrended Correspondence Analysis (DCA) was applied, which is recommended for the preliminary ordering of data [31,32]. The length of variance gradient calculated in this analysis characterizes the data structure and constitutes the criterion for selecting further ordination methods to assess the significance of the tested environmental or agrotechnical factors. Due to the fact that the length of the first axis gradient in DCA analysis was lower than 2 standard deviations, which showed that the distribution of species was not compatible with the Gaussian curve, linear method Principal Component Analysis (PCA) was used to perform direct ordination [33]. The results of this ordination were presented graphically on diagram (PCA diplot). The analyses were performed in the Canoco 4.5 program [32].

3. Results

3.1. Species Richness and Abundance

A total of 11 species of earthworms were recorded in the compared agricultural systems (Table 3). The largest number of species occurred in the willow (10 species), and the lowest number was in the high-input crop production systems: wheat monoculture and the conventional system (7 species). In the organic system, there were many juvenile unspecified individuals (Lumbricidae sp.). It should be noted that Allobophora chlorotica was found only in crop production systems on arable land and that Proctodrilus antipai was only found under perennial energy plants.
In crop production systems on arable land, the largest number of earthworm individuals (88.6 indv. m−2) was recorded in the soil under winter wheat cultivated in organic system (Table 3). Over twice less individuals (35 indv. m−2) were found in monoculture of winter wheat. Earthworms density decreased in the order of ORG > CON > INT > MON. Among compared energy crops, willow had the largest earthworm abundance (74 indv. m−2, only 16% less than in the organic system) while the smallest was found in miscanthus field (43 indv. m−2, 23% more than in wheat monoculture).
Total earthworm abundance was significantly higher in the organic system as compared to winter wheat monoculture (p = 0.001; z = 3.85) and to miscanthus (p = 0.008; z = 3.65) (Table 3). There were no significant differences between the organic system and willow in earthworm density.
Earthworm species number per sample was higher under winter wheat cultivated organically than under monoculture (p = 0.002; z = 2.68), than the integrated system (p = 0.045; z = 3.64), and than under miscanthus (p = 0.039; z = 3.24) (Figure 1). Earthworm diversity in the organic system and in Virginia mallow did not differ significantly. Among the tested energy crops, differences in the species richness were found between miscanthus and Virginia mallow (p = 0.032; z = 2.55).
The biomass of earthworms was 3 times larger in the organic system in comparison with the wheat monoculture, miscanthus, and willow systems (Figure 2). There were no significant differences between the organic, conventional, and integrated systems, which could be the result of using compost and catch crops twice in the integrated system and of using straw ploughing in the conventional system (Table 1).

3.2. The Relationships between Agricultural Systems and Species Composition

In the organic system, the indeterminate individuals (Lumbricidae sp.), mainly juvenile (27%) and O. lacteum (26%), constituted the most numerous groups (Figure 3). The highest density of L. terrestris was found in the organic system and Virginia mallow. The earthworm communities in the integrated system and the wheat monoculture system were dominated by A. caliginosa (39% and 60% share, respectively). The highest share of A. rosea were observed in earthworm communities under miscanthus and willow. In the soil under willow and Virginia mallow, earthworms unspecified for species, mainly epigeic juveniles of low biomass, dominated. In the miscanthus cultivation, A. caliginosa and A. rosea were the most numerous.
In order to confirm the relationship between land use and the abundance of earthworm species, the ordination method PCA (Principal Component Analysis) was used (Figure 4).
Along the gradients of the axes of particular crop production systems, species most closely associated with a given type of farming and energy crop were grouped together (Figure 4). O. lacteum was most closely connected with crops cultivated organically. L. terrestris, A. longa, L. rubellus, and unidentified Lumbricidae sp. were located close to the gradients of the axes of the organic system and Virginia mallow, which indicates that they were characteristic for both crop production systems. P. antipai and A. rosea were strongly positively correlated with willow. Species on the left-hand side of the diagram in Figure 4—A. caliginosa, O. cyaneum, A. chlorotica, and A. georgii—were associated with more intensive farming systems (CON, MON, and INT) and miscanthus.
Gradients of the systems and the species distribution in Figure 4 showed similarity of the earthworm communities for the organic system and Virginia mallow (right, upper site of the diagram) and dissimilarities from other, more intensive crop production systems (INT and MON) as well as miscanthus (left, down site of the diagram). Along the gradient of axis I, the highest positive correlation between the tested systems and the location of species occurred for willo and negative occurred for wheat monoculture. The most positively correlated with the gradient of axis 2 was the organic system while that negatively correlated was willow (Table A1, Figure 4).
The hierarchical classification confirmed the similarity of the earthworm communities in the organic and Virginia mallow systems and their dissimilarity from integrated system, wheat monoculture, and miscanthus (Figure 5). In these analyses, the dissimilarity of earthworm communities under miscanthus from the other two energy crops and their similarity to wheat monoculture and the integrated system have been shown.

4. Discussion

4.1. Species Richness and Abundance of Earthworms

In tested farming systems, on arable land, and among energy crops, 11 species of earthworms were recorded. Neirynck et al. [34] and Pfiffner [5] have shown that, generally, in cropland, only from 1 to 11 species are commonly found from among the about 40 earthworm species occurring in Central Europe. Most of them are species with a wide range and large adaptation abilities. The most common species in Poland are Dendrobaena octaedra (Sav.), Lumbricus terrestris L., L. rubellus Hoffm., Aporrectodea caliginosa (Sav.), Aporrectodea rosea (Sav.), and Eiseniella tetraedra (Sav.) [26].
The relative abundance of earthworms depends upon soil type, topography, and vegetation, and it is influenced by land use [1,34]. According to Lavelle [35], in terrestrial ecosystems, density of earthworms may reach 106 ha −1 and their biomass may reach 2 t ha −1. They are present everywhere except in arid and frozen regions. In Central Europe, about 120–140 earthworms per 1 m2 of arable soil are considered satisfactory in terms of soil fertility [5]. In our own research, a smaller number of earthworms were recorded, i.e., between 88 indv. m−2 in the organic system up to 35 indv. m−2 in monoculture. The lower earthworm abundance could be the result of being sandier, having higher acidity, and having low humus content of the investigated soils compared to the other European countries, which are not favourable to earthworms [5]. Very low earthworm abundance on sandy soils was also observed on conventional arable dairy farm situated in Peer in the sands of the Campine region (Belgium) [36].
Almost all of the earthworm species found are typical of the region and land use [26]. A. caliginosa was most abundant in arable systems. It is a species found in a wide range of environments. It is highly tolerant of habitat quality, including acidification and low levels of organic matter. The species tolerates intensive tillage to some extent, making it the most common species on arable land. Other highly represented species, L. terrestris, O. lacteum, O. cyaneum, A. longa, A. rosea, and L. rubellus, have slightly higher habitat requirements and are typical rather for meadows and pastures habitats than for arable land [35]. The species with the highest tolerance for low pH is A. chlorotica, which was found to have one individual in a cereal monoculture. Among the rare species, A. georgii was found. This species was previously found in the neighbouring region of the Mazovian voivodeship [26]. A rare, South European species of the earthworm, P. antipai, is usually found on heavy soils in the Vistula river valley, whereas in the studies, it was found in poor light soil. Heavy hydrogenic soils also lie in the farm serving the experiments, which suggests that both species could be transferred with the soil on agricultural equipment.

4.2. The Effect of Crop Rotation and Catch Crops

The number of earthworms depends on the availability and quality of organic matter in the soil [6,26]. On the arable land, manure and compost as well as the protein-rich residues of legumes (Fabaceae) are particularly preferred by earthworms. A diversified crop rotation with long-lasting and deep-rooted catch crops rich in clover or green manure crops as well as diversified crop residues are essential to maintain or increase earthworm populations [5]. This was confirmed by our own results showing that earthworm species richness and density were significantly higher in the organic system than in other systems (by 126% higher mean number of species and by 156% more individuals than in wheat monoculture). The higher species number and abundance of earthworms in the organic system could be the effect of the diversified crop rotation with clover and grasses mixture as well as of the compost and catch crop used, which provided food for earthworms. In a study by Schmidt et al. [37], a wheat-clover cropping system supported earthworm communities that were twice as large and had between one and five times more earthworm species than that found under conventional wheat mono-cropping. The above authors recorded between one and five more earthworm species in the wheat-clover system than in the pure wheat system.
Increased earthworm density was also observed as a result of mulching of crop residues on the field surface, especially during winter [5,38]. Post-harvest residues are an important source of organic matter, and they also affect the microclimatic properties of the soil. In mulched soil, there are more earthworms feeding close to the soil surface. In addition, such soil is more resistant to freezing than the soil without plant cover, which has an impact on the mortality of earthworms during winter, late autumn, and spring [12]. In our study, larger number and biomass of earthworms in the conventional system than in the integrated system could have been caused by a large biomass of post-harvest residues from the incorporation of wheat and rape straw.
The content and type of humus in soil are some of the most important factors determining the species composition of earthworms. L. terrestris has a tendency to occur in soil rich in organic carbon [39]. In our own research, L. terrestris was the most frequent in wheat in the organic system and Virginia mallow, where the content of organic matter was the highest. According to Schmidt et al. [37], wheat-clover cropping especially favoured species belonging to the epigeic and epigeic/anecic ecological groups such as L. rubellus and juvenile Lumbricus and was also observed in our own study, whereas A. caliginiosa may occur even in soils poor in carbon [39]. In the presented study, A. caliginosa was the most numerous in the intensive systems on arable land: integrated, wheat monoculture, conventional, as well as willow. A higher share of species typical for meadows and pastures such as L. terrestris, O. lacteum, O. cyaneum, and A. longa in the organic system is the result of 1.5 years of clover and grass cultivation preceding winter wheat in rotation. During this period, species building permanent vertical tunnels are not disturbed by soil tillage and receive some fresh plant residues on the soil surface, which promote development of such earthworm communities [35].

4.3. The Influence of Different Farming Systems

The effect of farming systems on earthworm species richness is a result of different agricultural practices, such as of crop rotation, crop protection, and fertilization.
Application of pesticides in conventional crop production systems can decrease density and biomass of earthworm population [12]. Pesticides may disrupt enzymatic processes, increase individual mortality, decrease fecundity and growth, or even change individual behavior such as feeding rate [5]. Anectic earthworms such as L. terrestris are most susceptible to surface application of pesticides, which, in our research, corresponds with a higher density of this species in the organic system in comparison with other agricultural systems where pesticides were used. Since L. terrestris forms permanent burrows, it does not come into contact with subsurface soil in its burrows. However, this species collects plant residues and pulls it into its tunnels, which is why it is directly exposed to the use of pesticides. On the contrary, endogenic species such as A. caliginosa, which continuously extend their burrows as they feed in the subsurface soil, are the most susceptible when toxic pesticides are incorporated into the soil [5]. According to Irmler’s research [12], the change from conventional to organic management has positively influenced species that form deep tunnels such as L. terrestris. The conversion from conventional to organic did not significantly affect the species penetrating shallow, horizontal tunnels, such as A. caliginiosa and A. rosea.
Herbicides probably do not damage earthworms directly, but they can reduce earthworm populations by decreasing availability of organic matter coming from weeds on the soil surface [40]. According to some authors, soil fauna is more threatened by the use of insecticides than herbicides. Active substances, such as carbofuran, forat, and terbufos, used to control soil-dwelling pests are also extremely toxic to earthworms [41].
Some synthetic mineral fertilizers, especially ammonium sulfate, can be harmful to earthworm populations, probably due to an acidifying affect [5]. On the contrary, the use of manure increases both the number and biomass of earthworms in arable land [42]. This was confirmed by our own study where the earthworm density was significantly the highest in the organic system. Similarly, Pfiffner’s and Mader’s [43] studies showed that, in conventional fields, where mineral fertilization and integrated plant protection were applied, the number and biomass of earthworms was about 40% lower compared to the fields where mineral-organic fertilization and integrated plant protection was applied. However, in the organic system, the number of earthworms was additionally 80% higher and the biomass was 40% higher in comparison to the object with mineral-organic fertilization and integrated plant protection. Moreover, the quality and quantity of manure could be important factors affecting the earthworm population due to salinity stress [44]. In our study, earthworm abundance under the organic system was higher than under the integrated, conventional, and wheat monoculture systems by 56%, 36%, and 156%, respectively. Similarly, Pfiffner and Luka [45] found about a 50% higher abundance of earthworms in an organic system as compared to integrated ones. Comparisons between organic and conventional systems have shown from an 80% [43] to a 400% higher earthworm density in the organic system [14]. In our research, the biomass of earthworms was 3 times larger in soil under the organic system than in the wheat monoculture, miscanthus, and willow. Similarly, Henneron et al. [14] found a 3 times larger biomass of earthworms in an organic system in comparison with high-input conventional system. In the study by Pfiffner and Mäder [43], the difference in earthworm biomass between organic and conventional systems with mineral fertilization and Integrated Pest Management (IPM) was about 75% and only 35% when the conventional system with mixed mineral and organic fertilization and IPM was compared. Stopping the use of synthetic fertilizers and pesticides are important factors that stimulate the population size and condition of earthworms in the organic system [5,14,26]. In more intensive systems, simplified crop rotation and high input of synthetic fertilizers and pesticides negatively affected the earthworm populations [12].

4.4. The Influence of Perennial Energy Crops

The influence of perennial energy crops on fauna diversity depends on cultivated species and agricultural practices [23,46]. Our study showed that mean earthworm species number, density, and biomass in energy crops were intermediate between wheat in organic system and high-input, intensive wheat monoculture and were dependent on the type of energy crop. Among tested energy crops, Virginia mallow created the best habitat in terms of species richness and biomass due to high amount of crop residues suitable for earthworms. The small amount of plant residues in miscanthus resulted in low earthworm indicators and high similarity to intensive crop production systems. In Felten and Emmerling’s [16] research, the number of earthworm species under miscanthus was placed between intensively cultivated crops (rapeseed, cereals, and maize) and grassland/fallow. In comparison to annual cropping systems, miscanthus plantation enhanced higher densities and diversity of soil invertebrates but not of ground-dwelling invertebrates [47]. In miscanthus stand, earthworm diversity and abundance were improved in arable soils although biomass may be reduced through poorer food quality [48]. Miscanthus leaf litter does not provide a particularly useful food resource due to its low-nitrogen, high-carbon nature [49], and earthworms feeding on this kind of low-nitrogen material have been found in other studies to lose overall mass [50]. In contrast, though, the extensive litter cover at ground level under miscanthus compared to the bare soil under annual cereals was suggested to be a potentially significant advantage for earthworms in soil surface moisture retention and protection from predation [48].
Another study confirmed that miscanthus created a poorer habitat for fauna than did willow [51]. In our own research, earthworm density was the highest in the soil under willow. Studies conducted in Great Britain and Sweden confirmed the positive impact of willow on the diversity of invertebrates in comparison with crops cultivated in intensive conventional systems on arable land [19,52].
According to Hedde et al. [53], the change in land use from typical annual crops to perennial energy plants resulted in an increase in the density of invertebrates in the soil, which may be caused by a smaller amount of synthetic fertilizers and chemical plant protection chemicals used, with no significant changes in richness and species composition of tested invertebrates. In our study, earthworm indicators were dependent on the type of energy crop which correspond with our working hypothesis. In the cultivation of energy crops, more earthworms depended on the presence of mulch. L. rubellus as well as species that burrow deep tunnels, L. terrestris, A. longa, and O. lacteum, were present, which was also a consequence of the lack of tillage. The composition of earthworm species found in energy plants resembled that found in orchards [35].
Further research should be warranted to design and assess innovative cropping systems including the range of candidate bioenergy crops, possibly grown in alternative lands, and also in the face of future climate changes [54].

5. Conclusions

It can be concluded that the organic crop production system with a diversified crop rotation including grass-clover mixtures, catch crops, and manure application in the conditions of Eastern Poland (Central Europe) supported the largest diversity and abundance of earthworms in comparison to the high-input cereal monoculture and integrated systems. The organic system favoured the population of L. terrestris and juvenile Lumbricidae. The intensification of agricultural production by simplified crop rotation and the input of synthetic fertilizers and chemical plant protection products caused a decrease in the number of species and abundance of earthworms. A. caliginiosa dominated in the earthworm community in the monoculture of wheat. On plantations of energy crops, the earthworm population indices were located between the organic system and the high-input, intensive wheat monoculture. The effect of energy crop cultivation on earthworm abundance and ecosystem services which are provided depends on the respective crop species. Among the compared energy crops, Virginia mallow created the best habitat for earthworms. In miscanthus, earthworm community was the poorest and the most similar to wheat monoculture. The composition of earthworm species found in energy plants resembled that found in orchards. Proper management of energy crops can support biodiversity and ecosystem services supplied by earthworms, such as humus production..

Author Contributions

Conceptualization, M.M., J.S., and B.F.-S.; methodology, B.F.-S., P.R., and J.S.; validation, M.M. and J.S.; investigation, B.F.-S. and P.R.; data curation, B.F.-S. and P.R.; writing—original draft preparation, B.F.-S. and P.R.; writing—review and editing, M.M. and J.S.; visualization, B.F.-S. and P.R.; supervision, M.M. and J.S.; project administration, J.S. and M.M.; funding acquisition, J.S. and M.M.

Funding

The study was carried out under the statutory project of IUNG-PIB no 1.13. (2014–2017). This work has been cofinanced by the National (Polish) Centre for Research and Development (NCBiR) entitled “Environment, agriculture and forestry” project: BIOproducts from lignocellulosic biomass derived from MArginal land to fill the Gap in Current national bioeconomy, No. BIOSTRATEG3/344253/2/NCBR/2017.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Appendix A

Table
Table A1. Inter set correlations of agricultural systems variables with Principal Component Analysis (PCA) axes in study of earthworms communities.
Table A1. Inter set correlations of agricultural systems variables with Principal Component Analysis (PCA) axes in study of earthworms communities.
VariablesAxis IAxis IIAxis IIIAxis IV
ORG 10.41710.7252−0.05950.0732
INT−0.2282−0.1979−0.60130.0376
CON−0.06640.3486−0.2498−0.5203
MON−0.6226−0.0908−0.13630.4262
MIS−0.3108−0.15750.6736−0.5513
VIR0.15730.03990.50060.6283
WIL0.6536−0.6674−0.1273−0.0937
1 ORG—organic; INT—integrated; CON—conventional; MON—monoculture, MIS—miscanthus, VIR—virginia mallow, WIL—willow.

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Agronomy 09 00675 g001 550
Figure 1. Average earthworm species number per sample (0.0625 m2) in winter wheat cultivated in four crop production systems on arable land and perennial energy crops (average for 2014–2016, mean ± SE, n = 30). ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow. 1 Different letters indicate significant differences between treatments according to the Kruskal–Wallis test at p ≤ 0.05.
Figure 1. Average earthworm species number per sample (0.0625 m2) in winter wheat cultivated in four crop production systems on arable land and perennial energy crops (average for 2014–2016, mean ± SE, n = 30). ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow. 1 Different letters indicate significant differences between treatments according to the Kruskal–Wallis test at p ≤ 0.05.
Agronomy 09 00675 g001
Agronomy 09 00675 g002 550
Figure 2. Earthworm biomass (fresh weight g m−2) in winter wheat cultivated in four crop production systems on arable land and perennial energy crops (average for 2014–2016, mean ± SE, n = 30). ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow. 1 Different letters indicate significant differences between treatments within arable systems and energy crops according to the Kruskal–Wallis test at p ≤ 0.05.
Figure 2. Earthworm biomass (fresh weight g m−2) in winter wheat cultivated in four crop production systems on arable land and perennial energy crops (average for 2014–2016, mean ± SE, n = 30). ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow. 1 Different letters indicate significant differences between treatments within arable systems and energy crops according to the Kruskal–Wallis test at p ≤ 0.05.
Agronomy 09 00675 g002
Agronomy 09 00675 g003 550
Figure 3. Relative abundance of earthworms species in communities in different agricultural production systems. ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Figure 3. Relative abundance of earthworms species in communities in different agricultural production systems. ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Agronomy 09 00675 g003
Agronomy 09 00675 g004 550
Figure 4. Ordination diagram of agricultural systems and earthworm species abundance in relation to the first and second axes of PCA (PCA biplot). ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Figure 4. Ordination diagram of agricultural systems and earthworm species abundance in relation to the first and second axes of PCA (PCA biplot). ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Agronomy 09 00675 g004
Agronomy 09 00675 g005 550
Figure 5. The results of the hierarchical cumulative classification using the unweighted pair group method with arithmetic mean (UPGMA) of samples representing earthworm abundance in different types of land use using the quantitative Sorensen’s coefficient of similarity. ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Figure 5. The results of the hierarchical cumulative classification using the unweighted pair group method with arithmetic mean (UPGMA) of samples representing earthworm abundance in different types of land use using the quantitative Sorensen’s coefficient of similarity. ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Agronomy 09 00675 g005
Table
Table 1. Crop management in winter wheat in different farming systems and three perennial energy crops (2014–2016).
Table 1. Crop management in winter wheat in different farming systems and three perennial energy crops (2014–2016).
ItemsCrop Production Systems on Arable LandEnergy Crops
Organic (ORG)Integrated (INT)Conventional (CON)Monoculture (MON)
Cropspotato
spring wheat + undersown crop
clovers and grasses (1st year)
clovers and grasses (2nd year)
winter wheat + catch crop (mustard)		potato
spring wheat + catch crop
faba bean
winter wheat + catch crop (mustard)		winter rape
winter wheat
spring wheat		winter wheatmiscanthus (MIS),
Virginia mallow (VIR),
willow (WIL)
Soil tillage mouldboard ploughing0
Organic fertilizationcompost (30 t·ha−1) under potato + catch cropcompost (30 t·ha−1) under potato + 2 × catch croprape straw,
winter wheat straw		wheat straw (every 2 years)0
Mineral fertilization (kg ha−1):natural P and K fertilizers:
N08514080
P2O542556060
K2O75758080
Retardants01–2 x2 x0
Fungicides02 x2–3 x0
Weed controlweeder harrow 2–3 xweeder harrow 1 x
herbicides 1–2 x		herbicides 2–3 x0
Table
Table 2. Soil chemical properties of the 0–30 cm layer of Luvisol.
Table 2. Soil chemical properties of the 0–30 cm layer of Luvisol.
Cropping SystempHKClCorg (g kg−1 of Soil)PEgnerKEgnerMg
(mg kg−1 of Soil)
ORG 15.659.940.364.069.3
CON5.908.184.8164.050.1
INT5.758.185.4134.141.9
MON5.087.752.3111.746.5
MIS4.005.797.257.530.3
VIR4.605.882.4136.151.0
WIL4.206.677.2104.362.0
1 ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow.
Table
Table 3. Earthworm species and abundance of individuals (indv. m−2) in soil under winter wheat cultivated in different crop production systems and in perennial energy crops (2014–2016).
Table 3. Earthworm species and abundance of individuals (indv. m−2) in soil under winter wheat cultivated in different crop production systems and in perennial energy crops (2014–2016).
NoSpeciesCrop Production Systems on Arable LandPerennial Energy Crops
ORG 1INTCONMONMISVIRWIL
1.Aporrectodea caliginosa13.921.916.521.39.610.19.1
2.Allolobophora chlorotica00.500000
3.Aporrectodea georgii03.21.10000.5
4.Aporrectodea longa1.6000.52.70.51.1
5.Aporrectodea rosea5.34.82.72.18.53.79.6
6.Proctodrilus antipai00001.65.94.8
7.Lumbricus rubellus1.10.50002.71.1
8.Lumbricus terrestris15.52.17.51.62.713.310.7
9.Lumbricidae sp.24.015.515.53.26.916.533.6
10.Octolasion cyaneum4.32.110.71.13.21.60.5
11.Octolasion lacteum22.95.910.74.87.59.13.2
Total species number89778910
Abundance (indv. m−2)
(mean ± SE)		88.6 ± 10
b 2		56.5 ± 9
ab		64.7 ± 10
ab		34.6 ± 6
a		42.7 ± 7
a		63.4 ± 9
ab		74.2 ± 18
b
1 ORG—organic; INT—integrated; CON—conventional; MON—monoculture; MIS—miscanthus; VIR—Virginia mallow; WIL—willow. 2 Different letters indicate significant differences between treatments according to the Kruskal–Wallis test at p ≤ 0.05 (n = 30).

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Feledyn-Szewczyk, B.; Radzikowski, P.; Stalenga, J.; Matyka, M. Comparison of the Effect of Perennial Energy Crops and Arable Crops on Earthworm Populations. Agronomy 2019, 9, 675. https://doi.org/10.3390/agronomy9110675

AMA Style

Feledyn-Szewczyk B, Radzikowski P, Stalenga J, Matyka M. Comparison of the Effect of Perennial Energy Crops and Arable Crops on Earthworm Populations. Agronomy. 2019; 9(11):675. https://doi.org/10.3390/agronomy9110675

Chicago/Turabian Style

Feledyn-Szewczyk, Beata, Paweł Radzikowski, Jarosław Stalenga, and Mariusz Matyka. 2019. "Comparison of the Effect of Perennial Energy Crops and Arable Crops on Earthworm Populations" Agronomy 9, no. 11: 675. https://doi.org/10.3390/agronomy9110675

APA Style

Feledyn-Szewczyk, B., Radzikowski, P., Stalenga, J., & Matyka, M. (2019). Comparison of the Effect of Perennial Energy Crops and Arable Crops on Earthworm Populations. Agronomy, 9(11), 675. https://doi.org/10.3390/agronomy9110675

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