Rotation/Succession Systems Affects Springtails (Hexapoda: Collembola) Abundance in Cash Crops Under No Tillage Cultivation

Acknowledging the bio indicator importance of springtails (Hexapoda: Collembola) for soil quality, this study aimed to determine the abundance of these arthropods in different systems of rotation/succession with commercial and cover crops, while also verifying the agricultural factor associated to these arthropods’ population. In the Instituto de Desenvolvimento Rural do Paraná (IAPAR-EMATER), during six years, areas with differing crops in rotation/succession adopting the no-tillage system were studied. For each system, chemical analyses of the soil were conducted and the number of captured springtails in pitfall traps was counted. The phytosanitary products applied during the evaluations and the quantity of vegetal cover remaining after harvest were considered as well. No difference was found between the rotation/succession systems in relation to chemical soil attributes, however the largest number of springtails was found in crop covers from corn, Brachiaria sp., and canola. These crop covers, including wheat, resulted in the highest straw dry mass. When removing the system in which the predecessor crop had the highest quantities of fungicide application, a positive correlation (r = 0.63; p < 0.01) was found, between springtail abundance and highest amount of straw after the harvest. If no fungicide applications occur, the crops with the largest amount of vegetal cover favor springtail populations.


Introduction
The no-tillage system is largely adopted in Brazil, currently considered the main grain crop management system in the country. The wide acceptance is due primarily to the reduction in loss of soil caused by erosion and the benefits towards chemical, physical, and biological properties of the soil (Bolliger et al., 2006). The no-tillage system supports a gradual improvement of soil quality due to the increase in organic matter content and biological activities (Duda et al., 2003;Gatiboni et al., 2009).
Leguminous plants are commonly used for soil cover, but other plant families are also used to maintain adequate cover (Menezes et al., 2004). In rotation or succession systems plant diversity is desired, which result in large straw residue production, low decomposition rate, nutrient cycling promotion and biological nitrogen fixation (Leal et al., 2005).
The presence of vegetal cover and no-tillage systems favor the edaphic fauna, which result in a greater diversity of organisms when compared to conventionally cultivated areas Baretta et al., 2006;Gatiboni et al., 2009). This is closely related to the quantity and quality of organic residues available to organisms that inhabit the soil, directly influencing their abundance (Warren & Zou, 2002;Antoniolli et al., 2006).
Studies assessing different soil management systems' effects on the edaphic fauna, demonstrate that the most abundant arthropod orders are Acari, Collembola, Coleoptera, Hymenoptera and Araneae (Silva et al., 2013;Silva et al., 2015;Santos et al., 2016). Organisms capable of determining the quality or level of soil degradation are considered as bioindicators (Wink et al., 2005). Springtails (Hexapoda: Collembola) are small arthropods, wingless and part of the mesofauna and are among the most abundant invertebrates in the soil (Alves & Cardoso, 2016;Culik & Zeppelini, 2003). They are considered one of the main groups of organisms used as bioindicators (Rusek, 1998;Bellinger et al., 2020), as they partake in the physico-chemical processes of the ecosystem, fragmentation, decomposition, and mineralization of soil organic matter, and are very important in maintaining soil quality and consequent nutrient cycling (Jänsch, Amorim, & Römbke, 2005).
Due to the sensitivity to changes in the environmental conditions in soil management, crop cultivation and mainly to soil degradation, springtails could be used as bioindicators of changes caused by incorrect soil management (Damé et al., 1996;Bedano et al., 2016).
Considering that the populations of springtails are bioindicators of soil quality, the present study aimed to determine the abundance of springtails in different rotation/succession systems, including cash and cover crops, adopting the no-tillage system, as well as, the agricultural factors associated with this arthropods' population.

Characterization of the Experimental Area
The experiment was carried out at the Instituto de Desenvolvimento Rural do Paraná (IAPAR-EMATER) (IDR-Paraná) in Londrina, PR (coordinates 23°22′ S; 51°10′ W; 585 m a.s.l.). According to Köppen's classification, the region's climate is humid subtropical with hot summers (Cfa), with an average annual temperature of 21.1 °C and an average annual precipitation of 1639 mm (IDR-PR, 2020). The soil is classified as Rhodic Ferralsol with a very clayey texture (Santos et al., 2018).
The experiment stated in 2014, and during six years, different crops following a rotation and succession of commercial and cover plants were cultivated, always following a no-tillage system. Six different rotation/succession systems (treatments) were performed, including the most common production system in the northern region of Paraná, soybean followed by corn ( Table 1). The cash and cover crops were sown in plots of 25 m 2 (5 × 5 m), with four replicates, following a random block experimental design.

Crop Managements Conducted During 2019 and 2020
The crop drying before the sowing of every vegetable in the different rotation/succession system was carried out with the following herbicides: Glyphosate ® , Aurora ® and Assist ® . In every crop, except Brachiaria sp., seed treatment was carried out with Vitavax ® and Cruiser ® . The phytosanitary products applied to the crop predecessor to soybean in the 2019/2020 harvest are shown in Table 2. The specific details regarding the applied phytosanitary products are necessary, as many of these products can reduce the populations of springtails (Frampton & Wratten, 2000;Carniel et al., 2019).

Soil Chemical and Dry Straw Mass Analyses
In September of 2019, after the winter season and before sowing the soybean, a chemical analysis from a soil sample was taken from each plot in the different rotation/succession systems. With the aid of an auger, with four points per plot, the soil was collected at a depth of 0-10 cm and taken to the laboratory to determine the following variables: pH in 0.01 M CaCl 2 ; calcium (Ca), magnesium (Mg) and aluminum (Al) contents by the KCl 1M extractor; potassium (K) and phosphorus (P) contents by the Mehlich-1 extractor; potential acidity (H + Al) by SMP; total organic carbon (TOC) by the Walkley and Black method; cation exchange capacity (T) and base saturation (V) were also estimated (Pavan et al., 1992). The results of the chemical analysis of the soil are represented in Table 3.   Note. * n.s. indicates that it was not possible to verify a significant difference, Scott-Knott test (α = 5%).
During the soil collection, in an area of 0.5 × 0.5 m from each plot, a sample of straw from the predecessor crop was taken. These samples were dried in a forced ventilation oven at 60 °C for 72 hours to determine the dry mass.

Springtail Sampling
In the 2019/2020 harvest, when the soybean crop was in the V4 development stage, springtails were sampled using pitfall traps (De Camargo et al., 2015), which are consisted of cylindrical plastic pots (14 cm in diameter × 9 cm in height), containing 200 mL of aqueous solution with 1% formaldehyde and 1% detergent. In each plot, three traps were buried with an open end at ground level and remained in the field for 72 hours. Subsequently, the traps were removed, and the collected content was washed under running water in a set of sieves. The material retained in the sieves with a 5 mm mesh were discarded, the content retained in the 0.044 mm mesh sieve was conditioned in 70% alcohol and kept under refrigeration (< 0 °C), for later identification and quantification of the specimens, with the aid of a stereoscope microscope. Identification was performed up to Order as proposed by Rafael et al. (2012).

Statistical Analysis
The data collected of each chemical attribute of the soil, amount of straw from the crop prior to soybean cultivation and abundance of springtails were complacent with normality and homogeneity assumptions. After that, followed tests of variance, with means compared by the Scott Knott test at 5% significance. Pearson's correlation test (r) was performed between the amount of straw from the crop prior to soybean cultivation and the abundance of springtail.

Results
A total of 196,050 springtails specimens were collected, belonging to three taxonomic orders: Entomobryomorpha, Poduromorpha and Symphypleona. The order Poduromorpha was the most abundant, representing 87.6% of the specimens collected, followed by the order Entomobryomorpha and Symphypleona, representing 21.1% and 0.3%, respectively. In addition, the largest number of springtails were captured in the rotation/succession systems adopted in the T1, T3 and T4 treatments, between 21% and 22.5% of the collected specimens; however, the lowest amount was observed in T2, with 9.2% of the specimens collected (Table 4). The rotation/succession systems adopted in the T1, T3 and T4 treatments resulted in the greatest abundance of springtails, with average values of 10.3 to 11.0 thousand individuals collected, differing from the systems adopted in T2, T5 and T6, in which only 4.5 to 7.1 thousand specimens were collected (Figure 1).  Vol. 14, No. 1; rotation/succession systems adopted (Table 3), indicating that the differences observed in springtail abundance ( Figure 1) are related to other factors.
The loss of vegetal cover reduces the population and variability of species of springtails (Loranger et al., 1998), on the other hand, layers of vegetal cover favor the abundance of springtails (Jandl et al., 2003), due to better survival conditions (Moço et al., 2005), since the vegetal cover serves as a shelter for these organisms (Baretta et al., 2003) and the straw provides food for most organisms that live in the soil (Silva et al., , 2013, these vegetal cover benefits could explain the greater springtail amounts in the treatments with higher remaining straw, in accordance with the correlation found when treatment 2 was removed. Lucero et al. (2020), when evaluating the abundance of soil organisms with five different vegetal coverings, found that springtails were the most abundant organisms in the area with wheat cover and in the turnip/ryegrass consortium, differing from the results found in this study, since the smallest populations of springtails occurred when the predecessor crop was wheat (T2). However, when analyzing the history of predecessor crops to soybean, there is a greater application of phytosanitary products in the wheat crop, mainly fungicides (three applications of Nativo® + Mancozeb®). In addition, the shortest time elapsed between the application of fungicides and the gathering of springtails also occurred during the cultivation of wheat (Table 2).
Studies show that fungicides negatively affect springtails in laboratory tests (Frampton, 1998) and in field conditions in wheat crops (Frampton & Wratten, 2000). The indirect effect of the use of fungicides on the populations of springtails can be attributed to the elimination of many fungi, which serve as food for several species of springtails (Scheu & Folger, 2004;Sawahata, 2006). In addition, Carniel et al. (2019), found that the application of the fungicide Mancozebe® reduces the survival and reproduction of springtails.
The application of fungicides and the shorter time between the application and gathering of springtails, probably caused the population decline of these organisms, even under conditions of large amounts of straw that the wheat provided, justifying the results obtained in this work.
In general, the populations of springtails are influenced both by the vegetal cover and by the amount of fungicide applied on the soil. However, the use of the springtail populations as bioindicators of soil quality should be carried out with caution, since their populations may, in a short period of time, recover from disturbances caused to the soil, and not reflect a cumulative effect over several years. For a better indication of soil fertility, other attributes should also be monitored.

Conclusion
The largest springtails populations occur in the rotation/succession systems in which the preceding culture provides a greater vegetal cover amount.
Fungicide applications can reduce springtail population.
Cultivating Brachiaria sp., canola, corn and wheat provide greater amounts of straw, compared to the consortium of buckwheat with oats and common bean cultivation.