Swine manure application enriches the soil food web in corn and soybean production

Our results suggested that swine manure application enriches the nematode community in ways that conventional PK fertilizer or no fertilizer does not. In contrast, conventional PK fertilizer did not shift nematode community composition relative to unfertilized control. Swine manure application strongly and consistently increased extreme enrichment opportunist nematodes – c-p1 bacterivores – that thrive on abundant, simple resources and rapidly colonize an environment under those conditions. These enrichment opportunist nematodes provide important services such as nutrient cycling that mineralize nutrients, particularly P and K, into plant-available forms (Holajjer et al., 2016; Trap et al., 2016). This suggests manure application enriched the soil ecosystem compared with conventional PK fertilizer or no fertilizer, an assertion that was reinforced by a consistent increase in enrichment index values. The soil food web enrichment driven by manure application was likely due to the greater amount organic matter and nitrogen in swine manure compared with conventional fertilizer (Hernandez et al., 2007) providing resources for colonizer organisms including bacteria and bacterivores, particularly organic carbon sources, whereas conventional fertilizers contain few or no carbon sources (Wolf and Wagner, 2005).

In the two years of this study, the influx of resources from manure application affected only nematodes that are highly adapted enrichment opportunists. Manure application generally did not affect c-p2 bacterivores or fungivores, which are also enrichment opportunists (Bongers, 1990). Omnivores and predators, which are persister strategists, were not affected by manure or conventional fertilizer application and were not very abundant overall. Similarly, neither manure nor fertilizer application affected community structure – the relative number of trophic links in a system – based on structure index. Manure was only applied once in this study and impacts on the soil food web were observed for two years after application, which is a relatively short time period. Perhaps manure application would increase abundances of organisms higher in the food chain if given further time for resources to flow through the food web, and potentially repeated manure applications, through bottom-up effects. Further research would be needed to investigate this.

Similar studies have generally found swine manure products (Bulluck et al., 2002; Mahran et al., 2009; Renco and Kovacik, 2012; Grabau et al., 2018) or other organic fertilizer amendments (Briar et al., 2007; Hu and Cao, 2008; Overstreet et al., 2010; Treonis et al., 2010) enrich the soil food web relative to no fertilizer application or conventional fertilizers. A few studies have found that conventional fertilizers enrich the soil community and increase bacterivore abundances compared with unfertilized land in a similar manner to manure or other organic amendments (Okada and Harada, 2007; Zhang et al., 2016). Community maturity or structure was not measured in many similar studies, but when it has been measured, organic fertilizer application either had no effect on maturity (Briar et al., 2007; Treonis et al., 2010) or decreased maturity (Bulluck et al., 2002).

In many similar studies, manure application has generally increased abundances of all enrichment opportunists, including fungivores (Bulluck et al., 2002; Briar et al., 2007; Hu and Cao, 2008; Renco and Kovacik, 2012), and both c-p1 and c-p2 bacterivores when measured (Liang et al., 2009). In one study, swine manure application had a similar impact as that observed in this study, increasing bacterivore abundances consistently but generally not affecting other trophic groups (Grabau et al., 2018). Differences in source material for the organic fertilizers used in this study compared with many previous studies may partially account for these differences since fungi and fungivores are more abundant in soils amended with organic materials of greater C:N ratios and more recalcitrant organic material than bacteria and bacterivores (Broder and Wagner, 1988; Wagner and Broder, 1993). In this study and Grabau et al. (2018), anaerobically digested swine manure – not mixed with any recalcitrant organic material – was applied. The other previous studies used slightly different material such as raw, undigested swine manure (Bulluck et al., 2002); swine manure that was composted (Liang et al., 2009) or mixed with sawdust (Renco and Kovacik, 2012); or cow manure composted with straw (Briar et al., 2007; Hu and Cao, 2008). Composting swine or cow manure changes the chemical and nutrient profile of these products, notably increasing the C:N ratio compared with raw or anaerobically digested manure (Troy et al., 2012; Qian et al., 2014). Raw swine and cow manure also differ slightly in their chemical and nutrient profiles (Qian et al., 2014).

Manure application somewhat decreased overall herbivore abundance at 45 DAP suggesting swine manure may have had some nematicidal effects on herbivores abundances. However, swine manure had little effect on abundances of the economically important plant-parasitic nematodes found at the site, primarily SCN, although it alleviated SCN damage to soybean at the SCN-conducive site as reported in Bao et al., (2013) study.

The increase in enrichment opportunists, but not other trophic groups, is indicative of broader changes in community structure and the flow of nutrients through the soil food web with the addition of manure. Manure application shifted decomposition pathways toward bacterial channels and away from fungal channels based on the channel index which is similar to the results in other studies (Liang et al., 2009). Similarly, manure application dramatically increased FBPP – the ratio of fungivore and bacterivores to herbivores. Greater FBPP values are interpreted to indicate greater beneficial services relative to detrimental effects from the nematode community (Wasilewska, 1989) since fungivores and bacterivores provide beneficial services, such as nutrient cycling, while herbivores are detrimental for crop production. Manure application decreased community diversity because that treatment stimulated population growth of a few genera of extreme colonizers to the exclusion of other nematodes. A number of nematode community indices have been proposed (Bongers, 1990; Ferris et al., 2001), and it is relatively infrequent for FBPP to be included in nematode community studies (Bulluck et al., 2002; Hu and Cao, 2008; Renco and Kovacik, 2012). In this study, FBPP was as sensitive as or more sensitive than many other indices including enrichment, channel, and structure index and provided distinct information about nematode community structure.

The influence of manure application on colonizer nematode abundances and soil food web structure continued over a year following fertilizer applications indicating manure application had residual effects on soil biology. These residual effects are likely due to a combination of continued influx of resources from continued decomposition of organic matter in manure (Diaz et al., 2012) and residual differences in nematode abundances among treatments from the fertilizer application event at the start of the study. In general, nematode community responses to fertilizer application were relatively similar among sites and crop sequences in this study.

As stated in the introduction, a long-term goal of this study was to identify strategies that improve sustainability (long-term productivity while conserving natural resources) of corn-soybean systems, particularly biological aspects of soil quality. Manure application clearly affected the nematode community and soil ecology, and some of these effects were positive such as stimulating populations of bacterivores that are very important for nutrient cycling (Trap et al., 2016), and increasing the ratio of beneficial to detrimental nematodes. Some of these effects are generally considered negative such as decreasing diversity and maturity which may reflect a community that is less resilient and resistant. Crop productivity, a key component of sustainability, was also improved with manure application (Bao et al., 2013), although more work would be needed to quantify if increased productivity was the result of increased nutrient input, changes in soil biology or a combination of factors. Further research and analysis would be needed to fully determine if the changes in soil ecology observed in this study are positive or negative and the degree to which manure application is a sustainable practice, particularly over a longer period of continuous practice.

Our results suggested that short-term crop sequences have a much less substantial and consistent influence on nematode community composition than swine manure application. Soybean, particularly resistant soybean, tended to encourage bacterivore population growth relative to corn, but only near the end of the first growing season and beginning of the second growing season. Conversely, corn tended to encourage fungivore population growth relative to soybean late in the year following production of these crops, although this trend was reversed at the end of the first growing season. In Midseason 2010, decomposition pathways were more fungal-dominated than bacterial-dominated in corn relative to soybean production, which also reflects these differences.

In a long-term corn-soybean rotation study in Minnesota near the site of the present study, corn also favored fungivores while soybean favored bacterivores, but it often took multiple growing seasons for these differences between cropping environments to be detectable (Grabau and Chen, 2016c). That trend is consistent with the relatively weak cropping effects in this study following only a single year of different crops. Differences in crop residue composition (Broder and Wagner, 1988; Halvorson and Schlegel, 2012), crop nutrient uptake (Halvorson and Schlegel, 2012), or root exudate profiles (Arafat et al., 2017) between corn and soybean may contribute to differences in nematode community composition in the presence of these crops (Grabau and Chen, 2016c). Other studies also suggest that different crops favor different groups of organisms resulting in varied soil community composition, particularly after cropping systems are implemented for a number of years (Briar et al., 2012; Djigal et al., 2012).

Crop sequences also affected total herbivore abundances during portions of the study with abundances greater under corn or susceptible soybean variously during the study. Based on the results reported in Bao et al. (2013) study, spiral nematode and SCN J2 abundances generally drove these trends as SCN J2 abundances were consistently greater in susceptible soybean rotation and spiral nematode abundances were greater in corn-soybean rotation than soybean toward the end of each year. Because overall herbivore populations were generally lower in resistant soybean than one or both of the other rotations, services provided by the nematode community were skewed toward beneficial and away from detrimental based on FBPP. This is similar to results of other studies (Grabau and Chen, 2016c).

Finally, our results suggested that short-term crop sequences and fertilizer application do not have an interactive effect on the nematode community. This implies that differences in nutrient uptake of fertilizer, soil food web composition, and other factors between corn and soybean did not alter the influence of fertilizer application on the nematode between these crops, at least in the short term. As discussed for fertilizer and crop sequence main effects, the lack of interaction may be due to the short-term nature of both the crop sequences and fertilizer application in this study. A hypothesis to investigate in the future is that long-term combinations of crop sequences and manure application exert a stronger influence on the nematode community than either practice on its own.

In conclusion, short-term crop sequences and fertilizer application did not have an interactive effect on the nematode community. Swine manure enhanced populations of extreme enrichment opportunist nematodes and enriched the soil food web relative to no fertilizer or conventional PK fertilizer. Manure application did not affect other groups of beneficial nematodes and decreased soil food web diversity, so impacts were a mixture of positive and negative. The nematode community was similar without fertilizer and with conventional PK fertilizer. Crop sequences drove some changes in soil ecology, but crops had fewer short-term impacts than manure application.