1. Introduction
Cover cropping has long been used to reduce soil erosion in agricultural fields, and to retain post-harvest residual nutrients or add nutrients by fixing atmospheric nitrogen [
1]. Field crop producers typically plant cereal or cereal–legume cover crop mixtures to provide ground coverage during periods when cash crops are not in season [
2]. Cover cropping practices are diverse and vary according to land managers’ goals. For example, cover crops can be grown with cash crops as living mulches that exist throughout the cash crop growth cycle [
3] and as naturally senescing companion plants (dying mulches) that are timed to senesce at an ideal period during the cash crop cycle [
4]. However, most cover crops are planted in the fall and terminated chemically prior to cash crop planting in the spring. This is done primarily to reduce competition for resources with the main crop [
5]. Cover crop termination results in plant residue that remains on the soil surface. These surface residues vary in dry biomass that persists through the growing season partially based on total cover crop biomass that has accumulated just prior to termination [
6].
Cover cropping has emerged as a viable weed management tool in conservation agricultural systems. When cover crops are terminated in reduced- and no-till cropping systems, resulting residues help prevent weed establishment [
7,
8]. Thus, it has been well established that cover crop residue can influence weed populations [
9,
10]. Notwithstanding, variation in cover crop biomass may impact weed levels differently. Greater production of cover crop biomass can enhance weed suppression through greater residue coverage and length of residue persistence [
11]. Though several studies have investigated the impact of cover crop residue on weed establishment in succeeding crops, limited research has been directed at examining how this residue impacts arthropods in the subsequent cash crop. The additional vegetative biomass from cover crop residue could affect arthropod populations by altering the structural complexity of the habitat.
The effects of increased habitat complexity through greater vegetation diversity on arthropod populations within agricultural systems have been well studied [
12,
13,
14,
15]. Lawton and Strong [
12] provide a definition of habitat complexity where simple habitats are those with lower biomass and diversity of plant resources and architecture. Plant architecture may be described as the height, heterogeneity, and structural complexity of plant or plant material. As such, non-living ground coverage or cover crop residue can be a vital contributor to agricultural habitat complexity. When a cover crop is terminated, the resulting residue is projected to increase habitat complexity through soil coverage [
16,
17,
18]. Increased habitat complexity in agro-ecosystems is predicted to increase the diversity of arthropods within the habitat and the ability of natural enemies to control pest populations [
12,
13,
15]. The amount of residue that remains on the soil surface and contributes to habitat complexity can vary with cover crop species, method of termination, and time allowed for growth prior to termination [
10,
19]. Therefore, management decisions that affect the resulting biomass of residue from cover crops may also affect the composition of the arthropod community in the succeeding cash crop.
Several studies have shown that cover crops and how they are managed can influence arthropod populations in succeeding crops. Koch et al. [
20] compared the effects of early- and late-terminated winter rye (
Secale cereale) on foliar arthropod counts in soybean (
Glycine max). The presence of rye residue reduced potato leafhopper (
Empoasca fabae) density compared to the no-cover crop treatment. Similarly, lower numbers of thrips were found in cotton (
Gossypium hirsutum) when residues of rye or crimson clover (
Trifolium incarnatum) remained on the soil surface [
21]. However, Smith et al. [
22] measured variable responses of different herbivorous insects to cover crop residue, with the lowest numbers of potato leafhopper and highest bean leaf beetle (
Cerotoma trifurcata) and Japanese beetle (
Popillia japonica) numbers in rye/no-till soybean compared to conventional tillage and treatments where rye was completely buried or absent. In addition to herbivores, their natural enemies may be influenced by cover crop residue. Lundgren and Fergen [
23] found that autumn-planted slender wheatgrass (
Elymus trachycaulus) increased subterranean predator diversity in the following maize crop compared to maize planted into fallow soil. Conversely, natural enemies may be uninfluenced by cover crop presence. For example, Jabbour et al. [
24] found no effect of cover crop biomass on carabid numbers in soybean planted with a cereal cover crop on a two-year rotation with maize and soybean. Similarly, Blublaugh and Kaplan [
25] found carabid numbers unchanged by the presence of rye and vetch (
Vicia villosa) residue in soybeans.
Growers in USA can receive financial assistance to grow cover crops outside of the growing season through the United States Department of Agriculture’s Environmental Quality Incentives Program (EQIP) for any farms where cover crops are identified as a Best Management Practice for promoting environmental conservation. Certain states, such as Maryland, New Jersey, and Delaware, have state-led programs funded through EQIP that specifically promote planting cover crops to promote soil health and water quality. Specific management practices, with respect to when and how cover crops are terminated, vary widely among individual farm operations. Variation in cover crop management techniques can affect the amount of cover crop residue that remains on the soil surface [
10,
19,
26], which impacts the resulting habitat complexity [
18]. Variation in habitat complexity may alter the community composition of arthropods within soybean fields. In the Mid-Atlantic area, soybean producers typically terminate their cover crop with a post-emergent herbicide during early spring (early- to mid-April). However, other producers terminate their cover crop later in the season (mid- to late-May), which allows greater cover crop biomass accumulation.
Though several studies have investigated how the method and timing of cover crop termination impact weed populations in grain crops, the impacts of these practices on arthropod populations are less well understood. The cover crop termination date is a crucial management tool for maximizing the benefits of these practices in agroecosystems [
27]. As such, the overall goal of this study was to examine how different cover crop termination practices impact the foliar arthropod community within no-till soybean plantings. The cover crop termination practices chosen were designed to mimic some of the most common methods used by Mid-Atlantic soybean producers. Specific objectives were to compare the influence of termination method (chemical versus mechanical) and timing (early versus late) on arthropod populations. Barley (
Hordeum vulgare) was chosen as the test cover crop partially because of its popularity among producers. A 2005 survey found that barley was the third most popular cereal grain cover crop in Maryland [
28], behind wheat (
Triticum spp.) and rye, and approximately 9300 ha were planted with a barley winter cover crop in Maryland in 2013 [
29].
2. Materials and Methods
2.1. Experimental Site, Layout, and Treatments
Field experiments were conducted at the University of Maryland’s Central Maryland Research and Education Center at the Upper Marlboro (38.859698, −76.778067) and Beltsville (39.012184, −76.826370) farm sites in 2013 and 2014. Field sites were previously farmed on a two-year maize (Zea mays) and soybean rotation with the exception of Beltsville in 2013, which was previously planted with grain sorghum (Sorghum bicolor) as opposed to maize. Field sites in Upper Marlboro were surrounded by production maize plantings, and in Beltsville, study sites were bordered by wooded areas on one side and production maize on the other. Treatments were replicated four times and arranged in a Latin square design. Individual plots measured 12 m × 10 m and were separated by 6 m of natural vegetation that was regularly maintained with a rotary mower.
Each field experiment consisted of four treatments, including three cover crop termination methods and a fallow/bare-ground control. The three cover crop treatments included: (1) early-kill (EK), in which the cover crop was sprayed with post- and pre-emergent herbicides in mid-April; (2) late-kill (LK), in which the cover crop was sprayed with post- and pre-emergent herbicides in late May; and (3) flail-mowed (FM), in which the cover crop was sprayed with a pre-emergent herbicide and mowed in late May. An early-kill, flail-mowed treatment was not included in the experiment because mowing typically does not kill cover crops at early stages of development [
30] and farmers do not use this method. The bare-ground treatment (BG) remained fallow after the previous crop was harvested, and received the same post- and pre-emergent herbicide applications as LK.
Barley “Nomini” was planted with a no-till drill into EK, LK, and FM plots at a rate of 135 kg ha−1 on 21 September 2012 and 24 September 2013 at both locations. Gramoxone SL® (paraquat, Syngenta Crop Protection LLC; Greensboro, NC, USA) was applied as a post-emergent herbicide using a tractor-mounted sprayer at 1.17 L ha−1 at Beltsville and 2.34 L ha−1 at the Upper Marlboro location. Authority® First (sulfentrazone, FMC Corporation, Agricultural Products Group; Philadelphia, PA, USA) was applied as a pre-emergent herbicide at all field locations at 329 mL ha−1. Herbicides were applied using 196.4 L ha−1 of carrier water at Upper Marlboro and 233.8 L ha−1 at Beltsville. The EK treatment was sprayed with the post- and pre-emergent herbicide mixture on 15 April at Beltsville and 16 April at Upper Marlboro in 2013 and on 18 April at both sites in 2014. The LK treatment was sprayed with post- and pre-emergent herbicide mixture on the day soybeans were planted. The BG treatment received the same spray protocol as LK. The FM treatment was sprayed with the pre-emergent herbicide, and the cover crop was mowed on the day soybeans were planted.
The soybean was planted on 21 May at Beltsville and 20 May at Upper Marlboro in 2013 and 27 May 2014 at both sites. LibertyLink
® maturity group four variety Stine 42LD02 (Bayer Crop Sciences; DeWitt, AR, USA) soybeans were planted with a no-till drill (model 1005, Great Plains Ag; Salinas, KS, USA) at 411,840 and 384,384 seeds ha
−1 in 2013 and 2014, respectively. Soybeans were planted in wide rows (76 cm inter-row spacing) at Beltsville and narrow rows (18 cm inter-row spacing) at Upper Marlboro. The initial protocol called for planting soybean at 76 cm row spacing at each site during both study years. However, the soybean was inadvertently planted at 18 cm spacing at Upper Marlboro during 2013. As a consequence, we opted to maintain this spacing at Upper Marlboro the following year. Still, it was not believed that this would impact the outcome, as earlier studies conducted in Maryland showed no impact of row spacing on the arthropod fauna in early- or late-planted soybean [
31]. A late-season herbicide application of Ignite
® (glufosinate, Bayer Crop Sciences; DeWitt, AR, USA) was applied at 511 mL ha
−1 on 11 July 2013 and 2 July 2014 to all plots at the Beltsville location as a “rescue” herbicide treatment primarily for large crabgrass (
Digitaria sanguinalis). Soybeans were harvested at both sites using small plot combines, and yields were adjusted to 13% moisture. Data on soybean yields are presented in a separate manuscript. Specific spray, planting, and harvest dates are summarized in
Table 1.
2.2. Plant Biomass
Cover crop and weed plant biomass were measured for each plot just prior to termination to determine barley and weed biomass production in cover crop and BG treatments. All vegetation was clipped at ground level within three (2013) or four (2014) replicate 0.25 m2 quadrats randomly placed in each plot. Samples were collected immediately before cover crop termination. Samples were then air-dried at 21 °C for at least one week and weighed to determine plant dry biomass. Data on the persistence of cover crop residue were collected on a weekly basis, and are reported in a separate manuscript.
2.3. Arthropod Sampling
Arthropod populations were measured by sweeping soybean foliage weekly with a 38.1 cm diameter canvas sweep net. A sweep sample consisted of two sets of five sweeps performed down two randomly selected rows at a sweeping width of ~1 m. Rows were haphazardly chosen for each sampling event, while excluding edge rows within each plot. Sampling was initiated at five or seven weeks after soybean planting (R1 growth stage) and was terminated at week 14 (R5 growth stage;
Table 2). All sampling was conducted between the hours of 8:00 a.m. and 12:00 p.m. Arthropod sampling was carried out on eight dates in 2013, from 10 July to 30 August, and 10 dates in 2014, from 1 July to 3 September.
Sweep-captured arthropods were transferred into plastic zip-storage bags, sealed, and temporarily stored on ice in a portable cooler while in the field. They were then transported to the laboratory and stored in a freezer for later species identification and counting. Arthropod samples were sorted under magnification using a stereomicroscope and stored in vials containing 70% ethyl alcohol. Micro-parasitoid wasps were identified to the family level and placed separately in 85% ethyl alcohol for storage. Arthropod taxa were divided into predators and herbivores and grouped into six functional feeding guilds and spiders. Insect feeding guilds consisted of chewing predators, sucking predators, parasitoids, plant-sucking herbivores, pod feeders, and foliar feeders.
2.4. Statistical Analyses
Arthropod feeding guild composition was analyzed using constrained ordination methods with the package vegan [
32]. Partial redundancy analysis (RDA) was used to determine the effect of cover crop treatment, soybean growth stage, and farm site on the overall composition of arthropod feeding guilds, while accounting for differences across years. Monte Carlo permutation tests were performed to test the significance of the multivariate model and each explanatory variable. Plant biomass of cover crop residue and winter weeds (fallow) and individual arthropod feeding guilds were analyzed with linear mixed models using the package lme4 [
33]. Plant biomass was analyzed with treatment, farm site, and their interaction as fixed effects, and year as a random effect. Arthropod feeding guilds were analyzed with treatment, soybean growth stage, and farm site as fixed effects, and block and treatment as nested random effects to account for repeated measures over time. Mean abundances were calculated for soybean growth stages that spanned multiple sampling dates. Multiple means comparisons were performed for significant terms from the mixed models, using Tukey-adjusted
p values. All data for arthropod abundances were log
10 (x + 1) transformed to meet assumptions of normality and homogeneity of variances. Reported means are from untransformed data. All analyses were performed using the statistical program R [
34].
4. Discussion
The objective of this study was to quantify the impact of cover crop termination method and timing on the arthropod community within soybean foliage. Cover crop termination practices are known to impact invertebrates via resulting residues that remain in the cropping system [
35]. Thus, it was hypothesized that different cover crop termination methods examined during this study would influence the arthropod community disparately. As projected, delaying the cover crop termination date resulted in significantly greater biomass of residue in late-kill (LK) and flail-mowed (FM) than in early-kill (EK) treatments. Averaged across years, delaying cover crop termination in FM and LK increased barley biomass relative to EK by 2007.5 kg ha
−1 at Beltsville and 716.8 kg ha
−1 at Upper Marlboro. Thus, it was hypothesized that this increased plant density and/or complexity would result in a concomitant increase in the number of predators such as spiders [
36,
37,
38]. It was unclear if termination method (mechanical versus chemical) would cause differences in the community of foliar-dwelling arthropods. Additionally, the fallow (BG) treatment, which had some weeds prior to herbicide application, had limited amounts of plant residue remaining on the soil surface shortly afterwards. Thus, it was not anticipated that residue in BG would have a perceptible effect on arthropod numbers.
The total abundance of all feeding guilds within the soybean foliage responded similarly to treatments and their associated plant biomass distinctions. However, the arthropod community composition changed in response to soybean growth stage, which is a similar finding to that of Dunbar et al. [
39]. These findings did not support our hypothesis that increased cover crop residue would benefit the arthropod community. Chemical (LK) and mechanical (FM) termination tactics also had similar effects on the arthropod community. This suggests that whether cover crops are killed early or late, or chemically or mechanically by mowing, the resulting arthropod community composition will be similar. The LK and EK treatments represent some of the most widely used practices for cover crop termination by Mid-Atlantic soybean producers, with the majority of producers choosing to terminate their cover crop “early” (early April) as opposed to “late” (at soybean planting from mid to late May). The results of our study suggest that the two cover crop termination practices are likely to result in similar foliar arthropod communities during the reproductive stages of the soybean plant development.
Relatively few other studies have found strong effects of residue from fall-planted cover crops on the foliar arthropod community in the succeeding agronomic crop. Koch et al. [
20] found that fall-planted rye reduced the abundances of some herbivorous insect species on soybean plants, but did not significantly affect predacious species. Conversely, Hooks et al. [
40] found greater populations of spiders on soybean foliage in treatments with Italian ryegrass (
Lolium multiflorum) cover crop residue compared to treatments without cover crop residue, but did not measure any differences in herbivorous species. Other studies have found no consistent effect of cover crop residue on arthropod herbivores or predators within soybean [
39,
41] or maize [
39,
42,
43] foliage. However, several studies have found greater numbers of ground-dwelling arthropods in field crops with greater cover crop residue [
39,
44,
45,
46]. As such, it is possible that epigeal predators may have responded to cover crop residue differently than those inhabiting soybean foliage.
Cover crop treatments from this experiment may have failed to have an effect on the arthropod community for several reasons. The amount of residue produced by the barley cover crop may not have been sufficient to influence the arthropod community within the soybean canopy. Studies investigating the effect of cover crop residue on the resulting arthropod community often do not report the biomass of cover crop residue, which makes it difficult to determine whether there is a minimum amount of residue required to significantly alter the arthropod community. Further, pest pressures at study sites may have been too low to detect any perceptible treatment effect or an associated numeric response from predators.