TY - JOUR AU - McMechan, Anthony Justin AB - Abstract Cover crops (CC) support populations of pest and beneficial arthropods. The status of these arthropods in the subsequent cash crop depends on several factors such as CC species, management, biomass production, and weather conditions. A systematic review was performed to identify how CC management influences pest and beneficial arthropods and to identify knowledge gaps for the future research efforts. Eight studies included in this review indicated that CC increase beneficial arthropods or some beneficial arthropods compared with the CC managed fields. A minority of the studies indicated an increase in pest presence when using CC. Cover crop species, termination time and methods, and CC management had variable responses on arthropod activity-density. The variable responses, differences on study designs, and complexity of CC management influence arthropod activity in a CC-corn [Zea mays L. (Poaceae)]/soybean [Glycine max L. (Fabaceae)] system, limiting our ability to draw a broad and effective conclusion about the CC management impact on arthropods. Local research studies are needed to identify the impact of CC biomass quality and quantity, CC biomass thresholds for pest and beneficial arthropods, and cash crop yield impact of CC management-arthropod-related studies. Studies using the standard farming practices of each U.S. region and using standard measurements are needed to guide farmers that use cover crops. This systematic review aims to provide a better understanding of how the complexity of management in cover crop-corn/soybean management affects arthropod activity-density and to identify potential gaps in research and address future research needs. Cover crops (CC) have increased in acreage across the United States as a sustainable means of improving soil health and suppressing weeds. Farmers using CC are hoping to enhance ecosystem function, that is, improve the capacity of natural processes to provide good services that satisfy human needs such as soil health, reduce runoff from fields to surface waters, and obtain weed suppression through plant competition (Bottenberg et al. 1997, Daily 1997, CTIC 2017). A 2016–2017 survey conducted by the USDA Sustainable Agriculture Research and Education (SARE) Program found that CC acreage in the United States increased from 383,523 to 606,760 acres between 2014 and 2016 (USDA-NASS 2017). According to USDA/NRCS, CC consists of ‘crops including grasses, legumes, and forbs for season cover and other conservational purposes’. Cover crops can be planted with a cash crop or after the crop is harvested, and typically consist of winter-hardy grains [cereal rye (Secale cereale L. (Poaceae)] and winter wheat [Triticum aestivum L. (Poaceae)], winter-killed grains [oats (Avena sativa L. (Poaceae)], winter-hardy legumes [hairy vetch (Vicia villosa R. (Fabaceae)], red clover [Trifolium pratense L. (Fabaceae)], and sweet clover [Melilotus officinalis L. (Fabaceae)], and forage covers [turnips (Brassica rapa L. (Brassicaceae)], rapeseed [Brassica napus L. (Brassicaceae)], and radishes [Raphanus sativus L. (Brassicaceae)] (USDA-NASS 2017). Relative to monocultures, the use of CC increases the plant diversity within an agroecosystem, which could attract both pest and beneficial insects (Bugg 1991, Landis et al. 2000, Tillman et al. 2004, Lundgren and Fergen 2010, Koch et al. 2012, Dunbar et al. 2016). The risk of pest transition from CC to corn system based on CC species and CC termination time was reported by Carmona et al. (2019). On the other hand, an increase in density-activity of Carabid beetles, which are generalist predators and also weed seed feeders, has been reported when using CC (Shearin et al. 2008). Decomposer arthropod communities, also considered beneficial arthropods, are expected to be affected by the rate of the CC decomposition (Rivers et al. 2018), but limited research has been done to address this matter. According to the USDA Natural Resources Conservation Service (NRCS) Cover Crop Termination Guidelines (USDA 2014), the United States is divided into four CC management zones. Management zones range from terminating the CC 35 d before planting the cash crop (western United States) to terminating the CC within 5 d after planting (the eastern United States except for Florida). These management guidelines use soil water availability to the subsequent cash crop as the main criteria for the termination of a CC. However, the risk for pest movement from the CC to the cash crop is not considered in the NRCS CC termination time recommendation. Cover crops should be terminated when the biomass production brings the maximum benefit to the cropping system, according to the grower’s goal. The termination can be done before, at, or after the cash crop planting date. Even though growers plan the termination date and follow the NRCS termination guidelines, weather conditions play an essential role in CC termination efficacy. Thus, it is important to have studies representing different scenarios in different regions of the United States to help growers to make the best management decision. The longer the CC is present, the more biomass production occurs (Lawson et al. 2015). Consequently, termination dates (i.e., early or late) may affect pest and beneficial arthropods differently in the following cash crop through creating different habitats for arthropods. Cover crop termination method is a management tactic used by growers that results in the termination of the CC growth. Several different methods can be used to terminate CC. In conventional systems, herbicides are most often used. However, mechanical methods are an alternative for both conventional and organic systems. Some other examples include roller-crimping, tillage, and mowing. In some cases, the CC fails to survive the winter and are referred to as winter-kill CC, which would not require termination in the spring. Winter-kill CC such as oats may not provide as many ecosystem services or weed control in the spring compared with CC that survives during the winter. In this context, each CC termination method influences how long the CC residue will persist on the soil surface, which affects the resulting habitat complexity. Each management strategies to terminate CC might have different impacts on different arthropod species before and after the CC is terminated. The relationship between CC and arthropods is not well understood, likely due to many potentially interacting factors involved in managing CC such as CC species, termination method, biomass production, and environmental conditions. The use of different CC practices is diverse and will vary according to the farmer’s goals. Over the past few decades, a handful of CC studies have shown the potential to increase the abundance of natural enemies and other beneficial arthropods, leading to a reduction in pesticide applications and increasing sustainability (Cardina et al. 1996, Landis et al. 2000, Shearin et al. 2008, Dunbar et al. 2016). In contrast, CC can also create an environment favorable for pest problems for the subsequent cash crop (Dunbar et al. 2016, Carmona et al. 2019). Dunbar et al. (2016) showed that CC might influence arthropod species differently. True armyworm [Mythimna unipuncta Haworth (Lepidoptera: Noctuidae)] larvae were significantly higher in corn [Zea mays L. (Poaceae)] fields following a CC of cereal rye. Black cutworm [Agrotis ipsilon Hunfnagel (Lepidoptera: Noctuidae)] larvae were higher in the CC fields but did not become a problem in the following corn crop. The abundance of common stalk borer [Papaipema nebris Guenee (Lepidoptera: Noctuidae)] larvae did not differ between corn fields following CC or not. Cover crop arthropod research has expanded in recent years out of the need to assess risks or benefits. Conducting literature reviews in the complex interactions of CC and cash crop management as well as varying response variables for arthropods makes a complicated environment to identify relevant studies. Under these circumstances, a systematic review offers a means of defining key characteristics in a system. Systematic reviews search, appraise, and collate all relevant information about a topic to provide a complete interpretation of the results and addressing future research needs (O’Hagan et al. 2018). A systematic review is performed based on eight steps: 1) formulate the review question, 2) define inclusion and exclusion criteria, 3) develop search strategy and locate studies, 4) select studies, 5) extract data, 6) assess study quality, 7) interpret results, and 8) disseminate findings (Uman 2011). In this context, a systematic review was conducted to synthesize the literature covering how CC management might influence arthropods in the subsequent crops of corn and soybean [Glycine max L (Fabaceae)] and determine what gaps exist in CC arthropod research. The specific objectives include 1) summarizing the relevant material and methods related to CC and arthropods as well as its value and limitations and 2) addressing the impact of CC management on i) total arthropod in the following cash crop compared with the non-CC treatment; ii) pest problems in the cash crop; and iii) beneficial arthropods (natural enemies and decomposers) in the cash crop. We hypothesized that 1) the use of CC would increase beneficial arthropods and decrease pest pressure in the cash crop and 2) CC management such as termination time, termination method, system, or other factors that increase plant density and/or complexity can provide a better habitat for beneficial arthropods. Materials and Methods Inclusion and Exclusion Criteria The following inclusion and exclusion were established prior to the literature search and review: Inclusion criteria: Paper included CC species. Paper included CC termination method and/or CC termination date. Paper describes a CC that is followed by corn, soybean, or wheat (Triticum aestivum (Poaceae)). Studies conducted in the field. Research results included arthropod measurement as a response variable. Field study conducted in the United States. Exclusion criteria: Publication before 1950. Publication other than article type. Papers that met all inclusion criteria were included in this systematic review. English-only publications were selected by using the language limiter available in each index. The exclusion criteria were met by using date and publication type limiters available in the databases. Literature Review Search Strategy Searches of the primary literature were conducted using the indexes CABI: CAB Abstracts and Global Health, Web of Science Core Collection, Scopus, and Agricola (via ProQuest). The search strategy used for each database was as follows: Topic 1=(cover crop* OR green manure * OR live mulch*) ANDTopic 2 = (insect* OR arthropod* OR arthropod pest * OR insect pest* OR predator * OR natural enem*) ANDTopic 3 = (crop rotation OR rotational cropping OR sequential cropping OR rotation OR cropping system*) ANDTopic 4 = (corn OR maize OR soybean OR soyabean OR wheat OR Glycine max OR Zea mays OR Triticum). In Web of Science and CABI, the search field was ‘ Topic’. In Scopus, the search field was ‘Article title, Abstract, Keywords’; in Agricola, it was ‘Anywhere’. In all databases, the document type was limited to articles and all topic were searched at the same time. Publication range was 1950–2019, except for the Scopus database, with coverage from 1989 forward. Scopus, CABI, and Web of Science searches were conducted on 31 July 2018, 15 May 2019, and 21 January 2020. The Agricola search occurred on 21 January 2020. Citations and publication PDFs were organized using ProQuest RefWorks (Cambridge Information Group, Bethesda, MD), and duplicates were removed. An Excel spreadsheet categorized the papers’ information and facilitated data visualization and organization (Supp Material I [online only]). In total, 304 unique papers were identified through the searches: 147 from CABI, 60 from Web of Science, 48 from Scopus, and 49 from Agricola (Fig. 1). Two hundred and thirty-one studies were excluded based on a lack of match to the search inclusion criteria, in an initial screen of title, abstract, and materials and methods. Full text of the 73 studies that initially met all criteria were accessed, and an additional 37 papers were excluded for not matching one or more criteria. Two papers, not identified through the database searches but considered important and meeting the search inclusion and exclusion criteria, also were included. The authors were aware of these papers, which had not been indexed yet by the databases. Fig. 1. Open in new tabDownload slide Illustration of screening steps applied to identify papers to include in the systematic review. Fig. 1. Open in new tabDownload slide Illustration of screening steps applied to identify papers to include in the systematic review. Results Description of Studies In total, 37 studies met the criteria for this analysis. Publication year ranged from 1983 to 2019 and generally reflected a low level of publication activity (Fig. 2). Studies were conducted in 15 different U.S. states (Fig. 3). According to the USDA-NASS (2017) Census Report, CC in the United States totaled 15.4 million acres in 2017. The three states with the highest CC area planted—Maryland (29%), Delaware (20%), and Connecticut (15%)—all border the Atlantic Ocean (Supp Fig. 1 [online only]). From the studies included in this review, three were conducted in Maryland and none in Delaware or Connecticut. Regarding the U.S. Midwest region, where the CC-corn/soybean/wheat systems are more common, Michigan had the highest CC area planted (8%), followed by Indiana and Ohio with 7% each, then Wisconsin with 6% (USDA-NASS 2017). Ohio was the Midwest state with most studies (6) published that were included in this review, followed by Iowa (5). The Midwest states with the lowest CC area planted in 2017 were North Dakota with 1%, Kansas (2%), and Nebraska (3%; USDA-NASS 2017). Surprisingly, after Iowa, South Dakota was the third Midwest state with the greatest number of papers published included in this review. Fig. 2. Open in new tabDownload slide Number of peer-reviewed papers published per year included in the systematic review. Fig. 2. Open in new tabDownload slide Number of peer-reviewed papers published per year included in the systematic review. Fig. 3. Open in new tabDownload slide Number of peer-reviewed papers published per U.S. state included in the systematic review. Fig. 3. Open in new tabDownload slide Number of peer-reviewed papers published per U.S. state included in the systematic review. Of the total studies (37), a majority (62.2%) were planted to a single CC species as expected, followed by a multispecies mix (21.6%). Only 16.2% of the studies examined both single and CC species mixes (Fig. 4A). Slightly more than half of the studies used grass species as CC (56.8%), a few used broadleaf (8.1%), and about a third a mix of CC species (8.1%; Fig. 4B). A survey performed by the SARE program and the Conservation Technology Information Center (CTIC) in 2017 reported that single species were more commonly used, followed by CC species mixes, and then CC broadleaf species. Fig. 4. Open in new tabDownload slide Summary of number of papers published by cover crop species (A) and type (B) included in the systematic review. Fig. 4. Open in new tabDownload slide Summary of number of papers published by cover crop species (A) and type (B) included in the systematic review. Sixteen different CC species were used among the 37 studies included in this analysis. Cereal rye (Secale cereale (Poaceae)) was the most used CC, followed by wheat (T. aestivum), and red clover (T. pratense; Fig. 5). In contrast, orchardgrass [Dactylis glomerata L. (Poaceae)], mustard [Brassica L. (Brassicaceae)], fescue [Festuca L. (Poaceae)], and buckwheat [Fagopyrum esculentum Moench (Polygonaceae)] were the least used. Research on these species partially aligns with a 2017 survey through by the SARE program and the CTIC where cereal rye was by far the most used CC in 2016 in the United States (289,068 acres), followed by oats (159,607 acres), radish (139,467 acres), and a four-way species mix (123,250 acres; USDA-NASS 2017). Cereal rye is among the most commonly used CC because of its ease of establishment, high biomass production, quick germination, relatively low seed price, and winter hardiness (Casey 2012). The same survey reported that the least-used CC species was canola [Brassica napus L. (Brassicaceae)] (14,503 acres), sunn hemp [Crotalaria juncea L. (Fabaceae)] (11,406 acres), and red clover (21,561). Fig. 5. Open in new tabDownload slide Summary of the 18 different cover crop species used among the studies included in the systematic review. Fig. 5. Open in new tabDownload slide Summary of the 18 different cover crop species used among the studies included in the systematic review. Eight different cover crop termination methods were identified (Fig. 6). As expected, herbicide treatment was the predominant method (37% of the studies), followed by forage harvest (17%), mowing (15%), rolling (9%), and disking (8%). Cut, plow, and tillage were among the least common methods used to terminate the cover crops, each method represented in only 2% of the studies. Eight percent of the papers did not mention the CC termination method used but mentioned the CC termination date, fitting the inclusion criteria for this review. Among the studies reporting the CC termination time relative to the cash crop planting, 35.7% terminated the CC before, 14.3% at, and 28.6% after planting the cash crop (Fig. 7). Fig. 6. Open in new tabDownload slide Number and percentage of studies using different cover crop termination methods. N/A represents information not provided by paper. Fig. 6. Open in new tabDownload slide Number and percentage of studies using different cover crop termination methods. N/A represents information not provided by paper. Fig. 7. Open in new tabDownload slide Number and percentage of studies terminating the cover crop before, at, and after planting the cash crop. N/A represents information not provided by paper. Fig. 7. Open in new tabDownload slide Number and percentage of studies terminating the cover crop before, at, and after planting the cash crop. N/A represents information not provided by paper. Fifteen papers (40.5%) had corn following cover crops and 14 (37.9%) had soybean (Fig. 8). The remaining studies had both corn and soybean as cash crops. There were no studies that met the inclusion criteria pertaining for wheat as a cash crop. However, wheat is the third most planted crop in the United States, following corn and soybeans. The lack of studies having wheat as cash crop indicates an opportunity for researches to study the use of CC in wheat as a cash crop systems. Fig. 8. Open in new tabDownload slide Number and percentage of papers using corn, soybean, or more than one cash crop following the cover crop. Fig. 8. Open in new tabDownload slide Number and percentage of papers using corn, soybean, or more than one cash crop following the cover crop. Several different sampling and evaluation methods were used in the studies and varied according to the study goals and objectives (Fig. 9). Fifteen studies used more than one arthropod sampling method. Pitfall traps were among the commonly used methods to collect arthropods, followed by arthropod assessment and crop injury caused by arthropods. In contrast, prey preference, predation bioassay, sentinel egg removal, and seed predation were the least used, representing more specific methods for evaluating certain arthropods. Fig. 9. Open in new tabDownload slide Sampling and evaluation methods to assess arthropods described in the papers included in the systematic review. Fig. 9. Open in new tabDownload slide Sampling and evaluation methods to assess arthropods described in the papers included in the systematic review. Cover crop variables varied greatly between studies with 17 testing more than one factor (Fig. 10). Among the total papers, 24 tested the differences between CC species, including the comparison of the treatments with and without a CC. Cover crop termination time was the second most common treatment variable (nine studies), followed by CC termination method (eight studies). Seventeen studies also used different system management such as differing nitrogen fertilizer rates, tillage (or disturbance levels), and insecticide and herbicide management. Studies focusing on only pest or only natural enemies represented 32.4 and 29.8% of the studies, respectively (Fig. 11). Only 24.3% focused on both pest and natural enemies, 8.1% sampled pest, natural enemies, and decomposer arthropods, and another 5.4% focused on natural enemies and decomposer arthropods. Supp Table 1 (online only) summarize authors, year, cover crop used, arthropod taxa examined, arthropod guild, sampling method, note on sampling method, cover crop effect on arthropod, note on the cover crop effect on arthropod, and cash crop yield reported in each paper included in the review. Fig. 10. Open in new tabDownload slide Treatment variable used per study to collect arthropods. In some studies, more than one treatment variable was used. CC, cover crop. Fig. 10. Open in new tabDownload slide Treatment variable used per study to collect arthropods. In some studies, more than one treatment variable was used. CC, cover crop. Fig. 11. Open in new tabDownload slide Number and percentage of arthropod groups focused on per study. Fig. 11. Open in new tabDownload slide Number and percentage of arthropod groups focused on per study. Arthropod Response Impact of Cover Crop Species Twenty-four studies had CC species as one of the treatment variables. The majority of those (16) had more than one treatment variable. As a result, some studies are also cited in other sections of this discussion. Cover Crop Versus No-Cover Crop Some studies (18) made conclusions based on a comparison to the non-CC treatment. Among those, several (7) found that with the addition of CC there was an increase in beneficial arthropods. Clark et al. (1993) reported that Staphylinidae (Coleoptera) and Lycosidae (Araneae) preferred the treatments with surface cereal rye residues over the fallow treatment. Shearin et al. (2008) found that ground beetle (Harpalus rufipes Latreille (Coleoptera: Carabidae) activity was three times higher in CC treatments (pea [Pisum sativum L. (Fabaceae)]/oat, cereal rye/vetch, clover/oat, and brassica/buckwheat systems) compared with fallow. Also, the carabid beetle H. rufipes released into the more diverse CC treatment (pea/oat–rye/vetch) were more likely to be recaptured in the same plot compared with its release in the fallow treatment, indicating a clear H. rufipes preference for habitats with more vegetation. Similarly, in 1 yr of their 2-yr study, Carmona and Landis (1999) found more carabid beetles’ activity-density in subplots with red clover compared to the no-CC treatment. For winter wheat as a cover, a significant increase in the numbers of the carabid genera Harpalus and Poecilus when compared with tillage (Davis et al. 2009). Altieri et al. (1985) and Lundgren and Fergen (2011) also provided evidence that the addition of CC positively affected beneficial arthropods, specifically by increasing predation levels, indicating that CC may provide an ecosystem service. Schmidt et al. (2007) found that the soybean following no CC had significantly lower natural enemy densities and diversity compared with the living mulch [soybean following alfalfa (Medicago sativa L. (Fabaceae)]. Similarly, an increase in abundance of predators and consumption of lepidopteran pupae was reported with the addition of living mulches of alfalfa and kura clover [Trifolium ambiguum M. (Fabaceae)] into corn and soybean, compared with the no-mulch (Prasifka et al. 2006). The use of CC increased the activity-density of some beneficial arthropod species measured, documented in three papers. Dunbar et al. (2017) reported a limited impact of fall-seeded cereal rye CC on beneficial arthropods; where Carabidae taxa was the only arthropod positively impacted when cereal rye CC was used relative to the no CC treatment. In the same study, Gryllidae was significantly reduced in plots with rye CC compared with the non-CC check. Similarly, Davis et al. (2009) indicated that the past presence of CC increased the number of the tested carabid species Harpalus and Peocilus, but not increased Amara and Anisodactylus species. Although not an arthropod, nematode community structure and complexity increased with CC use, but no consistent positive effect of CC on beneficial foliar soybean arthropods (Leslie et al. 2017). Three studies reported that the addition of CC decreased pest populations. The addition of cereal rye can reduce soybean aphid (Aphis glycines Matsumura; Hemiptera: Aphididae) pressure without reducing soybean yield (Koch et al. 2012). Koch et al. (2015) confirmed that cereal rye significantly suppressed A. glycines populations on soybean (in five of six locations), whereas A. glycines populations were 2.8–7.6 times greater on soybean grown without CC compared with CC. Similarly, Lundgren and Fergen (2010) found that wheatgrass [Thinopyrum intermedium Host (Poaceae)] reduced the third instar of western corn rootworm [Diabrotica virgifera LeConte (Coleoptera: Chrysomelidae)], and consequently, the root injury rating in the same treatment was lower compared with the no CC treatment in both years of the experiment. Additionally, they reported that predator abundance was strongly and negatively correlated with D. virgifera, implying that predation and direct effects of the wheatgrass as CC were both contributing to the decline in D. virgifera activity. On the other hand, three studies found that cereal rye as CC or wheat increased pest activity compared with the check (no CC; Hammond and Jeffers 1983; Hammond 1984, 1990). Seed corn maggot [Delia platura Meigen (Diptera: Anthomyiidae)] densities increased with cereal rye was incorporated, compared with the bare soil treatment (Hammond 1990). In previous work, Hammond (1984) found that D. platura numbers were very low when cereal rye was not present, compared with when cereal rye was used as CC. Finally, three studies indicated that the use of CC had a variable impact on pest arthropods. Smith et al. (1988) found that in some sampling dates, green cloverworm [Plathypena scabra Fabricius (Lepidoptera: Erebidae)], potato leafhopper [Empoasca fabae Harris (Hemiptera: Cicadellidae)], and striped flea beetles [Phyllotreta striolata Fabricius (Coleoptera: Chrysomelidae)] were higher in the rye-free treatment, whereas bean leaf beetle [Cerotoma trifurcate Forster (Coleoptera: Chrysomelidae)] and Japanese beetle [Popillia japonica Newman (Coleoptera: Scarabaeidae)] were higher in the rye no-till treatment. The authors concluded that it is unclear whether the CC can play a role in managing pests, as it will depend on the arthropod species and date of sampling. Dunbar et al. (2016) showed similar results, where cornfields with cereal rye CC had a greater abundance of M. unipuncta and consequently greater proportion of injured plants. However, P. nebris abundance did not differ between treatments with and without cereal rye, and A. ipsilon response varied between years. Buntin et al. (1994) reported that fewer corn plants were damaged by southern corn rootworm [Diabrotica undecimpunctata Barber (Coleoptera: Chrysomelidae)] following fallow and crimson clover [Trifolium incarnatum L. (Fabaceae)], whereas D. undecimpunctata damage in corn was highest after using hairy vetch. Different Cover Crop Species Cover crop species differ in their characteristics and can provide different resources to arthropods both before and after termination. Some herbivores may favor one CC over another, potentially altering prey resources for predators when different CC species are used. After the CC termination, the CC carbon to nitrogen ratio and the amount of lignin will dictate the decomposer community (Ruffo and Bollero 2003). To support the hypothesis that different CC species and CC mix would have varying effect on arthropod activity, ten studies compared how CC species might influence arthropod activity. The CC type (broadleaf or grass) and the plant growth status (living or death) impact on seed corn maggot a corn pest, is described by Hammond (1991). Based on orthogonal contrasts to test treatment relationships, the author noted a trend of higher D. platura populations in plots where a broadleaf (alfalfa or soybean residue) was incorporated in the soil, compared to when grasses were incorporated. The author found a trend of greater D. platura populations in plots with live, green CC (alfalfa or rye) incorporated when compared to a dead residue (soybean or corn). Higher survivorship of developing larvae or greater attractiveness of ovipositing females are discussed as possible explanations for higher seed corn maggot populations in the habitats previously mentioned. Two studies highlighted how the effects of CC species on arthropods are temporal in nature. According to House and Alzugaray (1989), the effect of CC species on soil herbivore populations was most pronounced early in the season. In April, they found that hairy vetch as CC supported more herbivore and predator populations, but there was no difference in the arthropod population when clover and wheat were used. In contrast, sampling in July found that wheat supported more arthropod herbivores and decomposer when compared to the other CC. Although Schipanskia et al. (2014) primarily studied how tillage intensity and initial CC impact corn productivity and the relationships between mediating ecosystem functions, the authors provide insights about initial CC species implications on arthropods. In a 3-yr conventional-to-organic system transition, predator activity-density was higher with the initial cereal rye/hairy vetch compared with timothy [Phleum pratense L. (Poaceae)]/red clover CC, but these effects did not persist into the third year. Three studies reported no consistent trends regarding CC species impact on arthropod activity. Leslie et al. (2017) tested how winter pea, barley, a winter pea-barley mix, and no CC influenced arthropod activity. They found a higher number of total predators in winter pea compared with the CC mix; however, more hemipteran predators were found in the CC mix compared with the barley treatment in one year of the study. Jabbour et al. (2016) and Roberts and All (1993) found no differences in arthropod activity-density between CC species used in their studies. Impact of Cover Crop Biomass Production and Habitat Complexity The biomass production potential of a cover crop varies considerably depending on the species. In addition, management practices, such as CC planting, termination, nutrient management, and environmental conditions, also influence CC biomass production and the habitat structural complexity created by CC biomass production. However, it is not known how CC biomass quantity and quality might influence arthropod activity. Most of the studies included in this systematic review did not measure CC biomass, except Buntin et al. (1994), Shearin et al. (2008), and Laub and Luna (1991). According to Buntin et al. (1994), cereal rye was the CC producing the most biomass (varied from 1,705 to 2,259 kg/ha), followed by crimson clover (from 893 to 1,946 kg/ha), wheat (from 662 to 976 kg/ha), hairy vetch (from 614 to 1,193 kg/ha), and fallow that was composed of weeds (from 203 to 243 kg/ha), depending on the growth season. However, they did not make any conclusion regarding the impact of biomass production on D. undecimpunctata activity or injury in corn. Laub and Luna (1991) planted a mix of cereal rye/hairy vetch at two seeding rates, 100.8/0.0 and 50.4/14.0 kg/ha, respectively. In their study, cereal rye/hairy vetch biomass production varied from 3,898 to 6,064 kg/ha with the 50.4/14.0 kg/ha mix, whereas cereal rye only treatments varied from 4,229 to 5,237 kg/ha. Similar to Buntin et al. (1994), Laub and Luna (1991) did not make an inference on how the CC biomass might affect the abundance of armyworm [Mythimna unipuncta Haworth (Lepidoptera: Noctuidae)]. Shearin et al. (2008) indicated CC biomass might influence arthropod activity. They stated that the pea/oat mix had more CC biomass (varied from 4,130 to 4,900 kg/ha of CC and from 1,320 to 1,630 kg/ha of weeds) and that this system attracted more H. rufipes during its CC phase and retained higher activity-density regardless of the residue management. Although CC biomass was not reported, two studies stated how more complex habitats created by using CC species mix could affect arthropod activity. Rivers et al. (2018) found that predatory arthropods, Araneae, Opiliones, Staphylinidae, and Carabidae, were more abundant when hairy vetch was planted with triticale (a more complex habitat) compared with the cereal rye treatment. They stated that the different habitat created in the different treatments (i.e., the amount of soil exposed, plant residue architecture, and biomass) provided different niches for specific taxa. Ward et al. (2011) found that in the treatment with higher dense canopy cover, the mustard/buckwheat/canola system had the highest numbers of carabid beetles captured in the study. Impact of Cover Crop Termination Method Eight studies included in this systematic review had CC termination method as at least one of the treatment variables. Six of the eight studies showed that a specific termination method affected the arthropods studied. Hammond (1984) compared a combination of the presence or absence of a cereal rye CC along with the use and the timing of an application of herbicide, paraquat (dipyridylium), and the type of tillage. He found that D. platura was significantly higher in plots where cereal rye was first plowed and then disked. Hammond (1990) compared CC residue and tillage (no-tillage and plowed) influence on D. platura. Delia platura was low in no-till and higher in treatments with incorporated residues. Rivers et al. (2018) managed hairy vetch-triticale and cereal rye with two termination methods, living or rolled, and three termination times (early, middle, and late). They found the CC termination method did not significantly affect arthropod activity-density, but specific arthropod taxa did vary by time in specific CC termination timings and methods. Bembidion quadrimaculatum oppositum Linaeus (Coleoptera: Carabidae), the most abundant carabid, and Chlaenius tricolor tricolor Dejean (Coleoptera: Carabidae), the second most abundant, were significantly positively associated with rolled hairy vetch-triticale, and with middle and late termination dates, respectively. Clark et al. (1993) determined the habitat preferences of generalist predators by comparing their abundance in reduced-tillage corn systems with different degrees of soil disturbance. They used three CC termination methods: roll, herbicide, and mowed/removed. They found that the predator abundance was higher in the CC terminated by rolling, followed by using paraquat, and then mowing. The carabids Pterostichus lucublandus Say (Coleoptera: Carabidae) and Pseudaptinus sp. (Coleoptera: Carabidae), the staphylinids Platydracus maculosus Granemhorst (Coleoptera: Staphylinidae) and Stenus flavicornis Ericheson (Coleoptera: Staphylinidae), and the spider Pardosa Koch (Araneae: Lycosidae) showed a preference for the cereal rye/roll treatment over the fallow/disk treatment. Laub and Luna (1991) evaluated the effect of two methods (herbicide and mower) of killing winter annual CC on P. unipuncta seasonal abundance. Herbicides type varies based on field location (atrazine, atrazine + prince, or cyanazine). Total P. unipuncta population in the mowed treatment was lower than in the sprayed treatment early in the corn season in three of the five fields. Laub and Luna (1992) studied the effect of spraying paraquat versus mowing the CC on predatory arthropods and parasitoids, and the relationship between predator abundance and P. unipuncta abundance. The authors found that CC that was mowed had a significantly higher number of generalist predators [Pterostichus spp. (Coleptera: Carabidae) and Scarites spp. (Coleoptera: Carabidae) and wolf spiders (Hogna asperse Sundeyall Araneae: Lycosidae)], playing a role in biological control of P. unipuncta. One study found no impact of the CC termination method on arthropods (Rosario-Lebron et al. 2018), and one study concluded the response of the CC termination method depended on the arthropod species (Smith et al. 1988). Rosario-Lebron et al. (2018) tested how different CC termination practices affect the foliar arthropod community within no-till soybean production. The CC termination method studied included using herbicide or fall-mowed. They found similar arthropod community composition when using either CC termination methods. Smith et al. (1988) compared different cereal rye CC management, disk, no-till, and no cereal rye influenced soybean foliage arthropods. The response of CC management depended on the arthropod species. Plathypena scabra populations varied during the 2 yr, with numbers in the cereal rye no-till being highest in the first year but lowest in the second year. Potato leafhopper [Empoasca fabae Harris (Hemiptera: Cicadellidae)] numbers were consistently lowest in the cereal rye no-till plots. In contrast, bean leaf beetle [Cerotoma trifurcate Forster (Coleoptera: Chrysomelidae)] and Japanese beetle [Popillia japonica Newman (Coleoptera: Scarabaeidae)] adults were highest in the cereal rye no-till treatments. Phyllotreta striolata were consistently higher in the conventional tillage and in the cereal rye plowed plots where cereal rye was completely buried or absent. Impact of Cover Crop Termination Dates Cover crop termination date guidelines are suggested by the Natural Resources and Conservation Services (NRCS). This guideline does not account for pest transition from the CC to the following cash crop. Thus, it is important to have studies representing different termination dates in different regions of the United States to support growers in making the best management decision. Even though 29 papers mentioned the termination time used, only five of those considered termination time as a treatment variable. Earlier research by Rivers et al. (2017) studied two termination dates; the first occurred before planting (late May) and the second, 7 d after the first, at planting date (early June). Their objective was also to determine the effects of CC management on the carabid community. The carabid activity significantly increased through termination time, where the late termination had higher activity than early termination. Another interesting result was the significantly lower proportion of small carabids such as B. quadrimaculatum oppositum, Bembidion rapidum LeConte (Coleoptera: Carabidae), Clivina bipustulata Fabricius (Coleoptera: Carabidae), and Bembidion mimus Hayward (Coleoptera: Carabidae) at late termination. The same treatment had a higher proportion of large carabids instead, such as C. tricolor tricolor, Poecilus chalcites Say (Coleoptera: Carabidae), Poecilus lucublandus Say (Coleoptera: Carabidae Latreille), Pterostichus melanarius Illiger (Coleoptera: Carabidae), Pterostichus mutus Say (Coleoptera: Carabidae), Cicindela sexguttata Fabricius (Coleoptera: Carbidae), and Harpalus affinis Shrank (Coleoptera: Carabidae). Many of the large carabids that were increased at late termination were predatory. In addition, species richness increased at late termination compared with early treatments. The results provide insights that CC termination timing might be a management strategy to influence carabid communities within the CC-cash crop system. Rivers et al. (2018) tested early, middle, and late termination of cereal rye (24 May, 29 May, 4 June 2013, respectively) and a mixture of hairy vetch and triticale (1 June, 6 June, 18 June 2013, respectively). They were interested in studying the effects of CC management on the arthropod community, focusing on ground-dwelling predatory organisms. The total arthropod activity did not vary with termination time, but they observed specific taxa varying throughout the different termination times. The carabid species B. quadrimaculatum oppositum was significantly more abundant in the middle termination date plots, while a second species, C. tricolor tricolor Dejean, was the most abundant at late termination areas. Each one of those carabid species is reported to consume different prey. There was also an association with high numbers of B. quadrimaculatum oppositum and C. tricolor tricolor with higher lepidopteran larvae and Collembola. The results indicate that prey availability helps determine the presence of these carabids at specific times during the season. Koch et al. (2012) monitored the soybean fields planted into cereal rye or no cover crop. They hypothesized that areas with cereal rye could reduce the population activity of insect pests, such as A. glycines, E. fabae, and Cerotoma trifurcata Forster (Coleoptera: Chrysomelidae). The treatments evaluated consisted of no cereal rye before soybeans, cereal rye mowed before soybean planting, cereal rye mowed after soybean emergence, and cereal rye mowed after soybean emergence but only between rows. The two locations where the study was conducted presented similar insect densities and dynamics during the experiment. The first sample date that captured A. glycines varied between treatments. Specifically, the treatment of cereal rye mowed between rows had a significantly lower number of A. glycines than areas with no rye. No significant differences in A. glycines numbers were found between termination dates. Empoasca fabae and C. trifurcata densities were significantly lower in the treatments with cereal rye compared with no cereal rye. In contrast, no differences were observed for these pests between the CC termination dates. The insect predators observed in the study included generalist insects such as Orius insidiosus Say (Hemiptera: Anthocoridae), Coccinellids, Nabis, and Chrysopids. The predator densities did not differ significantly among treatment or sample dates. Soybean yields were not significantly different between treatments at both locations. Even though insect pests were present throughout the experiment, pest pressure did not cause any measurable economic losses. Rosario-Lebron et al. (2018) also examined how CC termination date affects arthropod communities in a system with soybean as the cash crop. They compared early and late CC termination but did not find any impact on pest or beneficial arthropods. The late CC termination was done just prior to soybean planting and the arthropod community was not different between treatments. It is not possible to make conclusions about the effects on arthropods when CC is terminated after planting the cash crop because it was not tested. The risk of terminating CC after planting corn was reported by Carmona et al. (2019). In this survey, growers had early-stage corn plants infested by wheat stem maggot [Meromyza americana Fitch (Diptera: Chloropidae)] after using wheat or cereal rye as CC. The injured areas had in common the presence of green CC at the corn planting date, that is, CC was terminated after planting corn. The authors concluded that the corn infestation occurred as a result of dying cereal rye or wheat previously infested with the M. americana. With no food resources after CC died, the M. americana larvae migrated to the nearby corn plants to complete its development. Corn yield reduction of up to 30 bu/ac compared with areas with no CC was reported by growers, but not measured by the authors. Impact of Cover Crop-Cash Crop Rotations and System Management Growers may use several different cover crop to cash crop rotations systems, depending on their individual goals. Changes in these practices could alter the presence, activity, or abundance of arthropods. Such changes may include but not limited to fertilizer management, tillage system before and after CC establishment, herbicide rates for weed control, disturbance rates during CC-cash crop season, and insecticide management. Eleven studies had CC-cash crop rotations and/or system management as a treatment variable. To reduce any misunderstanding, study treatment nomenclatures as in the original publication were maintained. Fox et al. (2016) compared no-till corn without CC, no-till corn with CC, switchgrass [Panicum virgatum L. (Poaceae)], and a restored prairie to determine the effect of those systems on enhancing predatory communities and biocontrol services. The authors hypothesized that the no-till corn with CC system would have greater predator abundance. They also hypothesized that using CC would create a habitat that supports A. glycines populations and attracts mobile predators, serving as a source or sink habitat for predators. Contrary to their hypothesis, predatory abundance and diversity were higher in the perennial systems (prairie and switchgrass) compared with the annual systems (no-till corn with and without CC). In addition, they found that existing predator communities in CC treatment suppressed A. glycines population, limiting their attractiveness to mobile predators. In previous research, Roberts and All (1993) studied if selected sustainable practices, such as CC species and tillage practices (no-till and minimum-till), would affect fall armyworm [Spodoptera frugiperda Smith (Lepidoptera: Noctuidae)]. They found a higher number of S. frugiperda in the plow tillage treatment in both years of the study. Also, there was a reduction in the number of needed insecticide applications in the no-till plots with CC to control S. frugiperda compared with the plow-till plots. Davis et al. (2009) also studied tillage impact on arthropods, but in combination with cropping systems (amounts of residues), and different rates of herbicide treatments. They found that treatment impacts depended on the arthropod species. More activity of carabid beetles from the genera Amara, Anisodactylus, Harpalus, and Calathus and crickets were found in the no-till treatment, with or without CC, while wolf spiders (H. aspersa) were more abundant in weedier habitats with more ground cover. House and Alzugaray (1989) also found that the corn followed by hairy vetch under no-till system supported higher arthropod activity. Specifically, they stated that during early-season, no-till supported more predators; however, later in the season, there was no difference in arthropod activity between the no-till and conventional system. Moreover, the same authors found that D. platura was higher in the conventional treatment in 1 yr of the study. To test the hypothesis that invertebrate seed predator activity and predation rates would be higher in cropping systems with less soil disturbance and fewer chemical inputs, and longer ground cover during the season, O’Rourke et al. (2006) compared two cropping systems. A 2-yr corn/soybean rotation and a 4-yr corn/soybean/triticale-alfalfa/alfalfa rotation system. This study’s results failed to support their hypothesis. Specifically, their findings showed that Gryllus pennsylvanicus Burmeister (Orthoptera: Gryllidae) was the most abundant invertebrate seed predator and it was trapped more often in maize than soybean and least often in triticale–alfalfa and alfalfa treatments. Moreover, the predation of Setaria faberi Herm (Poaceae) seeds by invertebrates were higher in maize and soybean compared with triticale–alfalfa and alfalfa, and there were higher predation rates in reduced input (less herbicide and inorganic fertilizer amounts) compared with conventionally managed soybean. In a follow-up study, ground beetles were monitored in a conventional chemical input (2-yr, corn/soybean rotation) and a low input (4-yr, corn/soybean/triticale-alfalfa/alfalfa rotation system) to understand how cropping systems affect ground beetle activity-density. O’Rourke et al. (2008) found that Carabidae activity, diversity, and species richness were higher in the low input system. Adams et al. (2017) also tested systems that represent different levels of disturbance to compare the effects of it on soil and foliar arthropod abundance and diversity in soybeans and corn. The systems used in this study were conventional clean till, conventional long rotation, conventional no-till, organic clean till, and organic reduced till. The study suggested that lower management intensity, as organic practices or reduced levels of disturbance, in conventional systems could contribute to greater arthropod diversity. Shearin et al. (2008) and Ward et al. (2011) also studied how different levels of disturbance affect different species of ground beetles (Coleoptera: Carabidae). According to Shearin et al. (2008), some level of disturbance might benefit H. rufipes. Later research by Ward et al. (2011) found that carabid beetle activity varied between treatment, time of sampling, and year, but their findings suggest that CC positively affected carabid activity and when CC was not used, disturbance negatively affected the activity-density of A. aenea and Harpalus pensylvanicus Degeer (Coleoptera: Carabidae). Buntin et al. (1994) studied the cover crop species, nitrogen rate, and insecticide management effects on D. undecimpunctata damage in corn. Besides, the CC species impact on D. undecimpunctata discussed previously, the nitrogen rate did not affect D. undecimpunctata damage in corn. In addition, the authors found a highly significant interaction between crop and insecticide management, where the use of terbufos (organophosphate) as insecticide effectively prevented D. undecimpunctata damage and increased grain yield when clover and vetch were used as CC. Lundgren et al. (2013) studied how three pest management systems, chemically intensive, reduced chemical, and spring cover crop treatments affected insect populations. In addition, the authors looked at how the insects collected responded to the treatments between years. In the two chemical treatments, A. glycines were successfully suppressed. Insecticide applications from the chemical treatments (called reduced and intensive pest management systems) reduced bean leaf beetles and foliar-dwelling predators. Soil predator populations were mostly not affected by the different pest management systems studied. Hammond and Cooper (1993) studied the impact of time of insecticide application and time of soybean planting after the incorporation of CC. Phorate (orgaphosphate) insecticide treatment provided the best D. platura control. Soybean planting dates had little effect on D. platura abundance; however, low numbers were recorded in the latest soybean planting, 3.5 wk after the incorporation of the cover crop. Jabbour et al. (2016) conducted a cropping system study to determine the impact of initial CC species, soil management practice, and the transition start year on ground-dwelling arthropod abundance and diversity during the transition to organic production. The authors found that initial CC species, soil management practice, and year in which transition to the organic system was started had an effect on ground-dwelling arthropod activity-density. Cover crop species had the greatest influence on ground-dwelling arthropod activity-density in the first year of the transition. However, by the third year, tillage intensities and transition start year had higher influence on arthropod communities. These findings suggest that the management strategies during the transition from a conventional system to an organic system could be done in a sustainable way, conserving beneficial arthropods. Rivers et al. (2017) also studied the transition from a conventional to an organic system. The authors compared three CC termination and cash crop planting dates, crop rotation, and high residue cultivation on carabid beetles. Similar to Jabbour et al. (2016), Rivers et al.’s (2017) results also support that the system management, mainly plant residue, reduced tillage, and time of cover crop termination could have implications on carabid beetles during the transition to organic systems. Discussion As a field of research, CC are a complex platform of interacting factors that vary over time with changing agricultural practices. This system is further complicated by the myriad of different response variables that are used to estimate the presence or impact of pest or beneficial arthropods. The combination of these complexities results in a difficult environment for conducting a literature review of relevant research. To address this issue, we conducted a systematic review of the CC and arthropod literature using key search terms that were confined to the United States resulted in 304 unique papers. Inclusion criteria for cover crop characteristics and arthropods measurement resulted in 37 papers published between 1983 and 2019. Even with these inclusion criteria, these papers varied considerably in experimental design, use of control plots, plot size, biomass measurements, the inclusion of different arthropod species or groups, location, and management of the system, making it difficult to draw any broad conclusions. Of the studies reviewed, the most consistent response in arthropods and CC interactions was the increase in beneficial arthropods when using CC compared with a non-CC. From 18 studies comparing CC versus non-CC treatments, 11 studies suggested an increase in beneficial arthropod or decreased pest pressure when a CC was present. In contrast, only a few studies reported increased pest populations with CC. Such results confirm our hypothesis that CC biomass increased the presence of predators and natural enemies. However, from these 11 studies, seven studies focused exclusively on the presence of carabids. Future studies need to broaden the scope of arthropod communities that might be present or important in the CC system. Temporal arthropods collection varied between studies. Most of the studies (30) sampled arthropods more than once during the CC-cash crop season, between April and September. In CC-corn and soybeans systems, cold weather at the CC termination time can influence arthropod transition to the cash crops. Reporting environmental conditions during the arthropod’s assessment period, such as temperature and precipitation, would help readers to understand the specific environmental conditions during sample time that might be influencing arthropod activity. Moreover, environmental conditions varied between years, affecting arthropod activity and the likelihood of pest pressure during the CC-corn and soybeans season. Thus, multiyear studies are needed to address and capture pest pressure variation between seasons in CC-corn and soybean systems. Pest pressure varies between years due to environmental conditions and the CC management impact on pests is still unclear. Most apparent in the systematic review was the lack of measurement of CC biomass. Of the 37 studies, only three measured CC biomass. Two other papers stated that more complex habitats affected arthropods; however, CC biomass was not measured. Biomass measurements of CC are a standard in other disciplines for measuring the potential positive effects or negative impact of CC. If any consistent relationship between CC biomass and arthropod activity is determined, it could provide practitioners with the foundational information to assess risk or benefit in their system. Basic insect ecology would suggest that the quantity and quality of CC biomass could influence arthropod habitat. Future studies need to evaluate and measure CC as well as any weed biomass to contribute to a better understanding of arthropod interaction in the system. Cash crop yield was measured and/or reported in only five studies included in this review. Reporting cash crop yield is important to understand the economic impact of CC management and arthropods in the system, both pests’ issues, and also the benefits of ecosystem services of beneficial arthropods. Reporting yields is also a great way to communicate CC management impact on arthropods study results with growers. Growers are becoming more interested in CC and in contributing to a more sustainable agriculture. Reporting cash crop yield and understanding its relationship with the CC management-arthropods is a way to to assist growers in making informed decisions. The adoption and interest in cover crops have been on a steady increase over the past decade. This renewed interest reinforced the need to develop a consistent set of measurements and methods for experiments. Such standards would allow for a greater understanding of the influence of geographic and environmental interactions with arthropods in cover crop systems. These methodologies should include CC biomass at termination, pitfall traps to collect a broad range of arthropods, a quantitative assessment of pest pressure, and the subsequent cash crop yield. In conclusion, CC use has increased in the United States due to its benefits to the agroecosystem. The complexity of CC-corn and soybean systems drives the need for future research to address the knowledge gaps in this area. Growers are finding some management challenges to maximize CC benefits in their system. For example, growers using CC-corn or soybeans system usually have a short period between the cash crop seasons to grow CC. Late CC fall planting may happen due to delay in the previous cash crop harvest. Early spring CC termination can occur because of environmental conditions. These situations reduce the CC grow window and biomass production potential, consequently minimizing the ecosystem services benefits of using CC. Moreover, several extra management strategies need to be planned by growers, CC species selection, CC termination time and method, and others. As a result, more research is needed in the field of agroecology as described in previous paragraphs to support CC use and help farmers in making informed management decisions based on their goals and limitations. Supplementary Data Supplementary data are available at Annals of the Entomological Society of America online. Supplementary Fig. 1. Percentage of cover crop use per US state. Data source: 2017 USDA Censuses of Agriculture. Supplementary Table 1. Summary of authors, year, cover crop used, arthropod taxa examined, arthropod guild, sampling method, note on sampling method, cover crop effect on arthropod, note on the cover crop effect on arthropod, and cash crop yield reported in each paper included in the review. 1Natural enemies, pests, or decomposers. 2 + represents increase, - negative, 0 no impact, and +/- variable impact of cover crop on arthropod. References Cited Adams , P. R. , 3rd, D. B. Orr, C. Arellano, and Y. J. Cardoza. 2017 . 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A Systematic Review JF - Annals of the Entomological Society of America DO - 10.1093/aesa/saaa049 DA - 2021-03-12 UR - https://www.deepdyve.com/lp/oxford-university-press/does-cover-crop-management-affect-arthropods-in-the-subsequent-corn-b3orB7WVUL SP - 151 EP - 162 VL - 114 IS - 2 DP - DeepDyve ER -