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Macro-management of small scale processes in three agroecosystems
Jerry D. Glover*†, Sasha B. Kramer‡, John P. Reganold§, Tom Forge¶, Jennifer Moore-Kucera║,
Preston K. Andrews**, S. Tianna DuPont††, and H. A. Mooney‡‡
The Land Institute, 2440 E Water Well Road, Salina, Kansas, 67401; ‡Department of
International Studies, University of Miami, Coral Gables, Florida, 33124; §Department of Crop
and Soil Sciences, Washington State University, Pullman, Washington, 99164; ¶Agriculture and
Agri-Food Canada, 6947 Highway 7, Agassiz, British Columbia, Canada; ║Department of
Horticulture, Oregon State University, Corvallis, Oregon, 97331; **Department of Horticulture
and Landscape Architecture, Washington State University, Pullman, Washington, 99164;
‡‡
Department of Nematology, University of California, Davis, CA; §§Department of Biological
Sciences, Stanford University, Stanford, CA 94305
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or limited number of outcomes associated with crop yield. The use of synthetic fertilizers,
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especially for the supply of nitrogen,
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To whom correspondence may be addressed. Email: glover@landinstitute.org
Keywords: organic farming, microbial activity, integrated farming, soil food web,
nematodes, soil fertility, nitrogen cycling
Industrial farming practices generally focus on providing the inputs necessary for a single
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Abstract
Concerns about the ecological impacts of industrially intensive agriculture have, in part,
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resulted in substantial increased interest in alternative approaches to farm management. Although
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certified input requirements technically define organic practices, a central principle of organic
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farming—the “living soil” concept—is that the biologically regulated interconnections in the soil
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ecosystem play key roles in maintaining desirable soil physical and chemical conditions.
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Considerations of these linkages are less central in industrially intensive agriculture, in which
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specific properties, such as fertility and soil structure, are often considered separately from the
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soil ecosystem as a whole. Although studies have indirectly supported organic farming’s “living
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soil” concept, our three-year study measured linkages in the soil food web and between soil
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chemical, physical and biological properties in conventional, integrated and organic apple
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agroecosystems. Organic inputs resulted in larger nematode communities, the compositions of
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which indicated greater soil food web connectivity and overall resource abundance for soil
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biological communities. Nematode community assessments were reflected by the greater overall
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soil quality of organic plots as compared to conventional plots. Soil food web and soil property
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characteristics of integrated plots, with equal levels of organic and mineral fertility inputs, were
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generally intermediate between those of conventional and organic plots. Organic inputs also
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affected processes important in N cycling, resulting in more efficient denitrifying communities
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which have been shown to reduce N leaching losses. Soil property measurements were widely
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correlated with one another indicating that benefits of organic inputs extended through the soil
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ecosystem from the microbial communities to higher trophic levels and to soil chemical and
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physical characteristics. Our results show that, while nutrients taken up by crops may be
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essentially identical in final form whether originally supplied by organic or synthetic fertilizers,
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the pathways through the soil ecosystem along which the nutrients are transformed and delivered
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are different and those differences affect the soil ecosystem overall.
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Introduction
Humans are not naturally well endowed to manage the many dynamic processes involved in
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ecosystem functioning at the landscape scale. Many of the most important processes occur
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belowground and are mediated by micro- and meso-organisms, making them even more difficult
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to understand and manage effectively. This human limitation proves particularly problematic for
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farmers, typically managing their croplands on the scales of hectares and seasons, who now try
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to balance the need for high productivity with the need to maintain ecosystem health on
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approximately 15 million km2. Nitrogen cycling in agricultural systems typifies the problem.
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Microorganisms cycle nitrogen, a critical nutrient of typically low availability to plants, rapidly
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through many forms that are variously susceptible to gaseous, leaching or runoff losses or are
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available to plants.
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Support for organic agriculture has grown significantly during the past several decades,
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largely as a result of growing concern regarding farming’s increased reliance on purchased
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industrial inputs and their resultant negative environmental impacts (Kristiansen and Merfield
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2006). Although organic practices are technically defined by certified input requirements, a basic
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principle of organic management is that “production is to be based on ecological processes and
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recycling. Nourishment and well-being are achieved through the ecology of the specific
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production environment. For example, in the case of crops this is the living soil…” (IFOAM
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2006). Central to the “living soil” concept, which at least goes back to Lady Eve Balfour’s book
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(1943) of the same title, is the assumption that biologically regulated interconnections in the soil
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ecosystem play key roles in maintaining desirable soil physical and chemical conditions
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(Kristiansen and Merfield 2006).
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Under industrially intensive farming practices, such interconnections are often of less interest
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with specific properties, such as fertility and soil structure, treated separately from the soil
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ecosystem as a whole. For example, from the latter point of view, nitrate molecules taken up by a
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crop are the same whether they come from organic or synthetic fertilizer and therefore there is
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little meaningful difference between the two fertility practices. Proponents of the “living soil”
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concept, however, view the biological pathways along which the nitrate molecule is transformed
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from the organic form in the fertilizer as being the relevant difference. From this point of view,
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because of the complex connections within the soil ecosystem, organic fertilizers provide not
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only the required nitrogen to the crop but also supply crucial resources for communities of soil
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organisms that in turn will enhance other soil properties and reduce dependence on external
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inputs.
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Although studies have indirectly supported organic farming’s “living soil” concept by
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demonstrating that organic farming is viable and beneficial to soil health (Reganold et al. 1987,
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Mader et al. 2002, Pimentel et al. 2005), no study of which we are aware has measured the
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effects of management practices on the interconnections between soil properties and biological
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communities. Results of previous studies carried out at the study site central to this report
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demonstrate that organic practices result in the following: 1) higher soil quality (Glover et al.
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2000); 2) similar apple yields, enhanced apple quality, increased profitability, and reduced risks
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of negative environmental impacts (Reganold et al. 2001); and 3) qualitatively different
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microbial communities that reduce nitrogen losses relative to conventional systems (Kramer et
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al. 2006).
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For this three-year study, we assessed the impacts of three agroecosystems on soil food web
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conditions and used correlation analysis to assess connections between key soil chemical,
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physical and biological properties. Conventional, integrated and organic apple production
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systems were used to represent a range of widely used fertility and pest management practices.
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Integrated farming systems, widely adopted in Europe, are designed to incorporate components
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of organic and conventional management practices to optimize the ecological and economic
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performance of the system (Sansavini 1997).
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In the first two years of the study, 2000 and 2001, we assessed the effects of farm practices
on soil chemical and biological properties identified as important indicators of soil quality. In
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2002 we performed additional laboratory analyses to assess differences in nitrogen cycling
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processes and pools and assessed soil physical characteristics of each management treatment
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using a soil structure index. We then used correlation analyses of the 2002 data to determine
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significant relationships between soil chemical, physical and biological properties.
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Methods
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Study site
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This study was part of a 20-ha commercial apple orchard in Zillah, Washington (latitude 46
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30’N). The 1.7-ha study area consisted of four 0.14 ha replicate plots for each of three
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management treatments: conventional, integrated and organic. In May 1994, the study area was
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planted with ‘Golden Delicious’ apples (Malus x domestica Borkh.) on EMLA.9 rootstocks in a
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randomized complete block design (Glover et al. 2000, Reganold et al. 2001). Each plot in the
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study area contained four rows of approximately 80 trees per row trained on a two-wire trellis
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system. Trees were planted at a spacing of 1.4 m within rows and 3.2 m between rows for a
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density of 2240 trees per hectare. The site was irrigated with an under-tree sprinkler system to
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supplement an average annual precipitation of 20 cm of rain. Soil at the site is a coarse-loamy,
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mixed, mesic Xerofluventic Haplocambid (FAO:Haplic Cambisol). Prior to the installation of the
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experimental orchard the site had been in grass pasture.
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Farming system management
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Appropriate soil and weed management practices for organic, conventional, and integrated
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treatments were determined in cooperation with orchard managers and through consultation with
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local farmers and consultants. In 2000 and 2001, calcium nitrate [Ca(NO3)2] provided all the
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nitrogen for the conventional plots; nitrogen inputs to integrated plots were provided equally by
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Ca(NO3)2 and blood meal; blood meal provided the sole nitrogen source for the organic system.
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The amount of added N was the same in all three treatments and no N fertilizer was applied to
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any of the treatments in 2002. Pests and disease were managed in all three systems based on
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recommendations from a licensed Pest Control Advisor (Wilbur Ellis, Inc., Yakima, WA, USA)
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and the farm managers. The organic system received only inputs certified by the Washington
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State Department of Agriculture. The history of fertilizer and pest management inputs is reported
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elsewhere (Reganold et al. 2001, Kramer et al. 2006, Peck et al. 2006).
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Soil sampling and handling
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In mid August of 2000, 2001 and 2002, just prior to harvest, approximately 15 soil cores
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were collected from 0-7.5 cm and 7.5-15 cm within tree rows in each treatment plot and then
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bulked and homogenized so that there was one composite soil sample for each depth from each
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plot. Samples were then split into three portions, with one portion immediately air-dried for later
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analysis of soil chemical properties. A second portion was refrigerated moist for analyses of
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microbial biomass within 24 hours. Remaining sample portions were kept at 4OC prior to
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microbial activity and nematode composition analyses, which were performed within two weeks
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of collection.
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Nematode community structure
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Nematode analyses were performed on composite soil samples from the 0-15 cm depth
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interval in fall of 2000, 2001 and 2002. Baermann pans (16 cm diameter) were used to extract
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nematodes from 50 g subsamples of soil (Kimpinski 1993). Each nematode suspension was
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poured into a gridded counting dish and observed with an inverted microscope. Total nematodes
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were determined by counting the number of nematodes in one-tenth of the dish at 40X. Then, the
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magnification was changed to 400X and the first 100 nematodes observed in each sample were
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identified at the genus and family levels of resolution.
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Nematode counts for each taxon were converted to the number of nematodes per 100 g dry
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soil. The fine-stylet Tylenchidae were included as fungivores. While there is uncertainty
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regarding true feeding habits of the Tylenchidae as a whole (Yeates et al. 1993), field
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observations (Todd and Oakley 1996) and lab studies (Okada et al. 2002) strongly suggest that at
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least some key genera (e.g., Filenchus) are fungivorous.
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The nematode taxa were assigned c-p values from 1 to 5, corresponding to their positions
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along the colonizer-persister continuum of nematode life-history strategies (Bongers 1999).
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Ecological weightings were assigned based on c-p values and then Structure Index (SI), Channel
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Index (CI), and Enrichment Index (EI) were calculated as described by Ferris et al. (2001).
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Soil chemical, physical and biological properties
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A commercial laboratory (Soiltest Farm Consultants, Moses Lake, Washington) analyzed air-
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dried samples for organic matter content (Keeney and Nelson 1982) and nitrate nitrogen (Nelson
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and Sommers 1982) in 2000, 2001 and 2002. At the same times, we measured microbial biomass
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carbon and nitrogen using the chloroform fumigation incubation method (Howarth and Paul
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1994).
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In 2000, 2001 and 2002, we determined potential activity of L-asparaginase, an enzyme
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involved in nitrogen mineralization (Tabatabai 1994). In 2001 and 2002, we also used the
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potential activity of β-glucosidase, an enzyme involved in the hydrolysis of complex carbons, as
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an indicator of soil carbon mineralization (Eivazi and Tabatabai 1990). L-asparaginase activity
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was measured by determining the ammonia released following the 2 hr incubation of the soil
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samples in the presence of toluene, tris hydroxymethyl aminomethane (THAM) buffer (pH 10)
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and L-asparagine at 37 °C for 2 h (Tabatabai, 1994). β-glucosidase was determined by measuring
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the amount of p-nitrophenol released after a 1 hr incubation of 1 g soil with toluene, p-
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Nitrophenyl--D-glucopyraonisde and modified universal buffer (pH 6.0).
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Earthworm numbers were determined by hand-sorting three, 15 cm diameter by 15 cm long
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cores taken from each plot in mid-July of 2000 and 2001 (Blair et al. 1996). A visual assessment
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of the physical condition in the soil surface (0-7.5 cm) was made in 2002 using a structure index
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developed by Peerlkamp (1967) and modified by McLaren and Cameron (1990).
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Assessments of denitrification and nitrification potentials were made in 2002. Denitrification
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potential [overall nitrogen gas emissions, including nitrous oxide (N2O) and dinitrogen (N2)] and
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N2O potential were determined using the soil slurry method described by Cavigelli and
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Robertson (2000). Two 10 g subsamples from each pooled soil sample were placed in jars and
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amended with 15 ml of a 1 mM Na-succinate - 1 mM KNO3 solution to supply excess nitrate and
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carbon to the denitrifiers. The jars were then sealed and flushed with nitrogen to create anaerobic
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conditions. One of the two jars representing each system was supplemented with acetylene (10-
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15% vol/vol) to block nitrous oxide reduction; the other jar was not amended. Gas samples were
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then taken from each pair of jars at least 4 times over a two-hour incubation period. Nitrous
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oxide concentrations in the gas samples were immediately analyzed using a gas chromatograph
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with an electron capture device. From these assays, the relative rate of N2O emissions (rN2O)
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was calculated as the proportion of total gaseous N emissions released as N2O.
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Nitrification potential was assessed using the methods described by Hart et al. (1994) as
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follows: 10 g subsamples of soil from each treatment plot were added to flasks containing 100 ml
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of 1.5 mM (NH4)2SO4 solution, which was combined with phosphate buffers and adjusted to pH
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7.2 before adding soil. Slurries were shaken at high speed for 24 hours at room temperature.
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Aliquots of 10 ml were removed from slurries at 2, 8, 14, and 24 hours and centrifuged for
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several minutes to separate out the soil. The supernatant was then decanted, frozen, and later
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analyzed for NO3- by cadmium reduction in an autoanalyzer. Potential nitrification rates were
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calculated from a linear regression of NO3- concentrations over time.
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Potentially mineralizable nitrogen was determined in 2002 from unfumigated controls
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included in the microbial biomass assays and incubated for 10 days as described by Rice et al.
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(1996) and Parkin et al. (1996).
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Statistical analyses
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All nematode data were analyzed using a split-plot-in-time analysis of variance model. Soil
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property measurements for treatments were statistically analyzed using SAS Institute’s PROC
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GLM for a randomized complete block design (SAS Institute, Cary, NC). Pearson correlation
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coefficients and statistical p-values were determined for 2002 data using SAS Institute’s PROC
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CORR statistical procedure.
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Results and discussion
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Nematode community structure
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A large number of nematode species inhabit the soil ecosystem and represent a wide range of
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trophic levels. Because of their functional diversity, nematode populations may be used to
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evaluate the general structure and function of the soil food web even though it is comprised of a
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much larger number and diversity of organisms (Ferris et al. 2001). The quality and quantity of
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organic matter in soil ecosystems provides a bottom up control of soil food web dynamics.
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Consequently, differences in organic matter inputs among agricultural management practices
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will impact soil food web structure and function. Additionally the use of pesticides can affect soil
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food web structure by exerting both toxic and stimulatory effects on soil organisms at different
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trophic levels (Johnsen et al. 2001).
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No system-x-year effects were significant for any of the nematode parameters and the
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presented results focus on the main-factor effects of the farming systems (Table 1). Greater total
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abundance of nematodes in organic plots in all years indicates that organic management
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sponsored greater fluxes of energy and nutrients through the soil food web than conventional and
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integrated management. These differences likely reflect the differences in C inputs to the
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different systems. Organic plots were fertilized in 2000 and 2001 with bloodmeal (80% organic
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matter; 14.4% N), the integrated plots with a combination of bloodmeal and CaNO3, and the
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conventional plots with CaNO3 only. Additionally, organic plots had greater perennial grass
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cover in 2000 and 2001 than conventional plots, which received applications of glyphosate to
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inhibit grass growth. Integrated plots received fewer glyphosate applications than conventional
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plots but grass cover was reduced in comparison to organic plots. Although perennial grasses
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compete with trees for water and nutrients, their root exudates contribute organic carbon to the
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soil system and serve as additional energy sources for soil organisms (Glover et al. 2007).
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Because bloodmeal is a relatively labile, N-rich material, we expected to also see higher
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numbers of bacterivores in organic plots than in conventional plots. The fact that no differences
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were measured (Table 1) may be the result of sampling in autumn, several months after
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bloodmeal application. Earlier sampling might have revealed a temporary increase in
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bacterivores, particularly enrichment opportunists, in the organic system.
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Organic plots did, however, harbor more fungal and root-feeding nematodes than
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conventional and integrated plots (Table 1). Differences were likely due to increased C inputs
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from the bloodmeal as well as increased inputs of fine roots, root exudate-C and hyphae of
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arbuscular-mycorrhizal fungi originating from the perennial grasses which were more abundant
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under the canopy of organic trees than conventional trees.
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Three indices proposed by Ferris et al. (2001) can be used to interpret the functional
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significance of changes in nematode community structure: the Structure Index (SI), Enrichment
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Index (EI) and Channel Index (CI). The SI is a measure of the degree of representation of the
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community by higher-order feeding groups, particularly taxa with stable population dynamics
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typical of less-disturbed soil habitats. Higher SI values are generally correlated with greater
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diversity of taxa and are indicative of food webs with greater complexity or “connectivity” and
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more abundant resources supporting the higher-order trophic groups (Ferris et al. 2001). SI
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values coincided with the relative levels of organic fertility inputs with SI values highest in
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organic plots, intermediate in integrated plots and lowest in conventional plots (Table 1).
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The EI measures the extent to which the nematode community is dominated by bacterivorous
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and fungivorous taxa with enrichment opportunist ecological characteristics, and is indicative of
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pulse inputs of nutrient-rich organic material and increased bacterial production and nutrient
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mineralization (Ferris and Matute 2003; Ferris et al. 2001). The EI did not differ significantly
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among production systems (Table 1). SI:EI ratios were similar for all treatments and indicate,
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according to Ferris et al.’s (2001) food web profile assessment, N-enriched food webs subject to
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low or moderate levels of disturbance. This profile assessment fits expectations for a fertilized
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perennial cropping system.
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The conventional plots had greater CI values than the organic plots even though the organic
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plots had greater abundance of fungivores and root-hair feeders (Table 1). This discrepancy is
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explained by the fact that the large fungivore and root-hair feeder community in the organic plots
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was dominated by the fine-stylet Tylenchidae (primarily Filenchus, Aglenchus and Boleodorus)
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which were assigned c-p rankings of 3 and are not included in calculation of the CI (Ferris et al.
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2001). These nematodes were significantly more abundant in the organic treatment than in the
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conventional and integrated treatments (Table 1). In contrast, the fungivore community in the
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conventional plots was dominated by Aphelenchus and Aphelenchoides, which have c-p rankings
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of 2, are considered enrichment opportunist fungivores, and are included in computation of the
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CI (Ferris et al. 2001). The abundance of enrichment opportunist fungivores did not differ
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among cropping system treatments (data not shown).
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Soil chemical, physical and biological properties
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Organic and integrated systems maintained significantly higher soil organic matter levels in
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the surface 7.5 cm for all three years of the study and in the 7.5 to 15 cm depth in 2002 than did
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the conventional system (Table 2). These differences in organic matter content likely reflect
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differences in fertility and grass management and are consistent with differences observed in
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comparative studies of other organic and conventional farming systems (Mader et al. 2002,
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Pimentel et al. 2005).
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Differences in nitrate nitrogen levels between treatments were inconsistent from one year to
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the next (Table 2) indicative of the dynamic nature of this form of nitrogen. Conventional
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fertilizers often result in higher nitrate nitrogen levels than organic fertilizers. Organic plots in
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this study, however, had larger organic nitrogen pools, which can potentially provide more
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mineralizable nitrogen. The nitrogen in the bloodmeal applied to organic and integrated plots is
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also rapidly mineralized to inorganic forms that help to maintain adequate levels of available
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nitrogen. Leaf nitrogen contents indicated adequate nitrogen levels in trees in all treatments and
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did not differ between treatments (Kramer et al. 2006).
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Microbial biomass measurements indicate relative sizes of microbial communities. The
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organic treatment maintained higher levels of microbial biomass carbon (MBC) in the surface
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7.5 cm than integrated and conventional treatments (Table 2). Organic and integrated treatments
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resulted in higher microbial biomass nitrogen (MBN) levels than did the conventional treatment
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in the surface 7.5 cm in 2000. Levels of MBC and MBN were similar among the three treatments
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in 2001. In 2002, the organic treatment resulted in greater MBC and MBN in the surface 7.5 cm
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than the conventional treatment and greater MBN than the integrated treatment (Table 2). Both
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MBC and MBN generally dropped off dramatically in the 7.5 to 15 cm depth. The only
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significant difference between treatments at that depth was observed in 2001 with higher MBN
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in organic plots than in conventional plots.
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Phospholipid fatty acid (PLFA) analysis of microbial populations, determined for each
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management treatment in 2002 and reported by Kramer et al. (2006), indicated significant
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differences in microbial community composition between the organic and conventional systems
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with the integrated system compositionally intermediate. Kramer et al. (2006) also linked
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compositional differences to denitrification activity and found the organically managed soils to
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support more active and efficient denitrifier communities than the conventionally managed soils.
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Measured differences in microbial community sizes and compositions were consistent with
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differences in potential activity of soil enzymes important in C and N cycling (Table 2). L-
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asparaginase catalyzes the conversion of amino acids to ammonium and its activity has been
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shown to correlate with mineralized nitrogen uptake (Burket and Dick 1998). β-glucosidase
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activity indicates the soil’s potential to hydrolyze low molecular weight carbohydrates and
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release glucose, an important energy source for soil microbes (Eivazi and Tabatabai 1990).
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Organically managed soils exhibited significantly higher activities for both enzymes than the
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conventional treatment for all three years in the surface soil layer (Table 2) and had significantly
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higher activity levels than the integrated treatment in 2001 and 2002. Potential enzyme activities
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decreased in the subsurface soil layer (7.5-15 cm) in all treatments corresponding to the
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reduction in microbial biomass, also observed for all treatments. No significant differences in L-
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asparaginase levels were observed in the subsurface layer, except in 2002 when levels in the
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organic and conventional treatments were greater than in the integrated treatment. The organic
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treatment supported greater levels of β-glucosidase activity in the subsurface than did the
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conventional treatment in 2001 and greater levels of β-glucosidase activity than did the
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conventional and integrated treatments in 2002.
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Earthworms can enhance microbial activity by concentrating nutrients in digested soil, which
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when excreted is significantly higher in microbial biomass, organic matter and plant available
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nutrients than bulk soil (Edwards and Bohlen 1996). Organically managed plots contained
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significantly (p≤0.05) more earthworms, (105 earthworms m-2) than integrated (31 earthworms
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m-2) and conventional (23 earthworms m-2) plots in 2000. Earthworm numbers increased under
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all management treatments in 2001 and remained significantly higher in organic plots (472 m-2)
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than in integrated plots (226 m-2) and conventional plots (189 m-2). Earthworm numbers were not
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significantly different in integrated and conventional plots in either year. Although earthworm
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numbers provide less information on soil food web characteristics than do types and sizes of
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nematode populations, the greater earthworm numbers supported by organic management may
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be the result of larger pools of energy-rich root exudates provided by grasses in organic plots.
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These types of food supplies can often be the limiting factor for earthworm populations (Linden
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et al. 1994).
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Soils managed under organic practices had significantly (p≤0.05) higher Peerlkamp structure
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index ratings (8.63) than did soils managed under integrated (7.04) and conventional (6.23)
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practices. Higher Peerlkamp ratings indicate greater organization of soil aggregates into larger,
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more stable macroaggregates. Such structural development results in soil bulk densities and pore
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size distributions more conducive to holding and releasing soil moisture and to enhanced root
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growth. The higher structural ratings for the organically managed soils are consistent with past
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measurements of greater soil aggregate stability and lower bulk densities (Glover et al. 2000).
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In 2002, we assessed the influence of management treatments on potential rates of
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denitrification, nitrification and N2O emissions and on potentially mineralizable nitrogen pools to
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determine if observations of greater enzyme activities were reflected in differences in soil
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nitrogen cycling processes. Organically managed soils exhibited significantly higher potentials
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for denitrification and N2O emissions than soils under conventional and integrated management
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(Table 3). We measured higher levels of mineralizable N in organic plots (11.3 mg N kg-1 soil) than
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in conventional plots (6.9 mg N kg-1 soil). Levels in integrated plots (10.6 mg inorganic N kg-1 soil)
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did not significantly differ from levels measured in organic and conventional plots.
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Organic management, however, resulted in roughly half the relative rate of N2O emissions
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(rN2O) than integrated and conventional management, indicating that a greater percentage of
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nitrogen gas emitted from organically managed soils is emitted as harmless dinitrogen (N2)
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(Table 3). Denitrifier communities in organically managed plots were nearly twice as efficient as
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those found in the integrated and conventional treatments, with 38% of gas being emitted as N2O
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in the organic compared to about 73% in the conventional and 78% in the integrated systems
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(Table 3).
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These differences in denitrifier community function may have important implications for
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nitrogen pollution. Although the organic soils exhibited higher potential rates of nitrogen
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cycling, a detailed field study of nitrogen losses following fertilization (Kramer et al. 2006)
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revealed no differences in soil N2O emissions among the different treatments in this orchard, but
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N2 emissions, which do not serve as greenhouse gases, were significantly higher in the organic.
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Kramer et al. (2006) also found annual nitrate leaching was 4.4 to 5.6 times higher under
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conventional plots than in organic plots, with the integrated plots in between. These field results
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point to the importance of denitrification efficiency in mediating the composition and
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environmental impact of nitrogen gas losses.
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Correlation analyses
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Overall, organic management practices enhanced soil biological activity as compared to
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conventional practices as indicated by a range of soil organisms, properties and processes.
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Effects of integrated practices on the soil system were intermediate between those of organic and
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conventional practices. While these results indicate farming practices do impact the “living soil”
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and that organic practices have positive impacts when compared to conventional practices, they
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provide little evidence of direct links between the “living soil” and the ecological processes upon
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which organic production is conceptually based.
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Correlation analyses of the 2002 data, however, do indicate strong links between many of the
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soil organisms, properties and processes included in this study (Table 4). Organic matter levels,
368
soil structure ratings and denitrification potentials were most strongly correlated among
369
themselves and with other soil properties and processes. Soil organic matter content is widely
370
considered an important indicator of soil quality and its influence on other soil chemical,
371
biological and physical properties is well established (Brady and Weil, 2008). A soil’s physical
372
structure is highly influenced by a soil’s organic matter content and biological activity and serves
373
as a solid indicator of positive or negative impacts of management practices on soil biological
374
activity, all other factors being equal.
375
While organic matter and soil structure, properties that usually take more time to improve
376
than most other soil properties, were expected to correlate well with biologically related
377
properties and processes, the high level of correlation seen between denitrification potential and
16
Glover et al.
378
all the other soil properties, except for NO3-N concentrations, was not expected (Table 4). Its
379
close link to other soil properties suggests that as the size and activity of the soil’s biotic pool
380
changes, the composition of biological communities also changes. The data indicate that
381
denitrifier populations increase disproportionately relative to increases in size and activity of the
382
soil’s biotic populations.
383
This concept is supported in several ways. For example, the ratios of denitrification potential
384
to microbial biomass carbon (DP/MBC) and L-asparaginase activity (DP/L-asp) are significantly
385
(p≤0.05) greater for organically managed soils (DP/MBC = 0.24; DP/L-asp = 1.04) than soils
386
under integrated (DP/MBC = 0.11; DP/L-asp = 0.52) and conventional management (DP/MBC =
387
0.03; DP/L-asp = 0.21) practices; values for integrated soils are also significantly greater than
388
those for conventional soils. The higher DP/MBC values indicate that a higher proportion of the
389
microbial community is able to denitrify in the organic soils (Groffman and Tiedje 1989, Kramer
390
et al. 2006) and the higher DP/L-asp values indicate greater denitrification rates for the whole
391
community for a given level of metabolic activity.
392
Additionally, Kramer et al. (2006), using PLFA analysis, found a qualitative shift in
393
composition of microbial communities in response to organic inputs in these same plots; in
394
addition, microbial communities in integrated plots fell between conventional and organic
395
communities. Perhaps indicating compositional shifts within denitrifier communities themselves,
396
rN2O measurements were negatively correlated with other properties and processes with the
397
exceptions of mineralizable N and NO3-N (Table 4). As biological community activities and
398
sizes increased, denitrifying communities were more efficient at reducing nitrogenous gases fully
399
to N2. Greater denitrification efficiency (lower rN2O values) can reduce greenhouse gas
400
emissions in agricultural systems (Kramer et al. 2006).
17
Glover et al.
401
Potential activities of the enzymes L-asparaginase and β-glucosidase were positively
402
correlated with most other soil properties and processes, except with NO3-N concentrations
403
where no correlation was seen (Table 4). Additionally, L-asparaginase activity did not correlate
404
with microbial biomass nitrogen nor did β-glucosidase activity correlate with nitrification
405
potential. The correlations between enzyme activities and sizes of biological communities and
406
organic matter levels indicate increased supplies of energy-rich food sources and support greater
407
internal nutrient cycling and recycling.
408
Microbial biomass carbon measurements correlated similarly well with other soil properties
409
although they were not correlated with NO3-N concentrations or with nitrification potential
410
(Table 4). As expected, microbial biomass carbon increased with organic matter content and
411
microbial activity. At the macro-scale, earthworm populations were only slightly less well
412
correlated with other soil properties. Surprisingly, earthworm numbers were not correlated with
413
NO3-N, mineralizable N or MBN measurements, all of which represent relatively dynamic pools
414
of nitrogen. In contrast earthworm numbers were highly correlated with nitrification potential, L-
415
asparaginase activity, denitrification potential and rN2O, all of which are associated with
416
nitrogen cycling.
417
It is also somewhat surprising that MBN measurements did not correlate with the other
418
closely related N pools of mineralizable N and NO3-N (Table 4) and, with the exceptions of
419
mineralizable N, nitrification potential and NO3-N, MBN measurements were the least well
420
linked to the other soil properties. Additionally, although they do correlate with NO3-N
421
concentrations, mineralizable N measurements do not correlate with nitrification potential. The
422
poor correlation between N pools and potential enzyme activities may be due to the relatively
18
Glover et al.
423
dynamic nature of inorganic N transformations which render single measurements poor
424
indicators of N status.
425
Conclusion
426
A key objective of organic farming is to maintain active communities of beneficial soil
427
organisms that regulate soil ecosystem processes necessary for successful crop production. A
428
basic assumption of this “living soil” concept is that significant interactions exist between soil
429
organisms and important soil processes and properties and that farm inputs can fundamentally
430
alter those relationships. Using conventional, integrated and organic apple production practices
431
to represent a range of farming practices, we investigated the validity of that assumption using
432
field and laboratory studies of nematode communities and a range of soil properties.
433
Organic inputs supported soil food webs with greater connectivity between trophic levels and
434
more abundant resources for fungal feeding nematodes. Soil food web conditions in integrated
435
plots were generally intermediate to those of conventional and organic plots, indicating that the
436
relative level of organic inputs was an important influence on the connectivity of soil food webs
437
and the pathways along which nutrients were cycled.
438
A wide range of soil physical, chemical and biological properties reflected the influence of
439
organic inputs on soil food webs. Soil quality, in general, was higher in organic plots than in
440
conventional plots and intermediate in integrated plots. Soil property measurements were widely
441
correlated with one another indicating that benefits of organic inputs extended through the soil
442
ecosystem from the microbial communities to higher trophic levels and to soil chemical and
443
physical characteristics.
444
Our results validate the idea that soil biological communities supported by organic inputs
445
benefit a wide range of soil properties important for agricultural production. One implication of
19
Glover et al.
446
these results is that, while nutrients taken up by crops may be essentially identical in final form
447
whether originally supplied by organic or synthetic fertilizers, the pathways through the soil
448
ecosystem along which the nutrients were transformed and delivered are different and those
449
differences affect the soil ecosystem overall.
450
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Table 1. Nematode faunal analysis by treatment, 2000–2002.
Treatment
Total
nematodes
Bacterial
feeders
Root hair
feeders
Fungal
feeders
Omnivores
and
Predators
Tylenchidae
Conventional
1084 a1
724 a
109 ab
57 a
45 a
150 a
Integrated
1064 a
770 a
44 a
64 a
60 ab
126 a
Organic
1916 b
985 a
226 b
385 b
79 b
240 b
1
Different letters within columns indicate significant differences between treatments (LSD;
p≤0.05).
25
Glover et al.
554
Table 2. Correlation between soil chemical, physical and biological properties in conventional, integrated and organic systems (0 – 7.5
555
cm depth). Coefficients with absolute values greater than 0.56 are significant at the 0.05 level (underlined) and coefficients with
556
absolute values greater than 0.49 are significant at the 0.1 level (bold font).
Ba
OP
NP
Min N
Pf
Ty
Βgluc
EW
rN2O
N2OP
Fu
TN
SOM
Lasp
MBC
SS
Denitrification. potential
0.32
0.65
0.69
0.62
0.51
0.59
0.78
0.91
-0.83
0.90
0.83
0.67
0.75
0.87
0.82
0.95
Soil structure
0.24
0.65
0.73
0.59
0.49
0.58
0.79
0.88
-0.82
0.84
0.80
0.60
0.80
0.81
0.86
Microbial biomass C
0.14
0.70
0.43
0.52
0.65
0.79
0.73
0.75
-0.75
0.68
0.76
0.58
0.79
0.73
L-aspariginase activity
0.17
0.38
0.65
0.50
0.60
0.56
0.77
0.92
-0.84
0.69
0.79
0.56
0.54
SOM
0.14
0.65
0.55
0.62
0.34
0.51
0.59
0.60
-0.59
0.77
0.49
0.40
Total nematodes
0.81
0.39
0.38
0.60
0.58
0.84
0.50
0.60
-0.68
0.56
0.74
Fungal feeding nematodes
0.24
0.65
0.60
0.47
0.81
0.72
0.52
0.87
-0.72
0.66
N2O potential
0.35
0.64
0.65
0.73
0.25
0.41
0.57
0.72
-0.54
rN2O
-0.36
-0.33
-0.60
-0.45
-0.60
-0.72
-0.88
-0.83
Earthworms
0.18
0.47
0.80
0.42
0.61
0.56
0.64
β-glucosidase activity
0.27
0.34
0.39
0.52
0.38
0.55
Tylenchidae
0.47
0.47
0.25
0.43
0.78
Plant feeding nematodes
0.03
0.58
0.23
0.20
Mineralizable N
0.51
0.45
0.28
Nitrification potential
0.17
0.19
Omnivores/predators
-0.03
26
Glover et al.
557
Figure 1. Non-metric multidimensional scaling (NMS) analysis of nematode genera extracted
558
from conventional (triangles), integrated (circles) and organic (squares) systems in 2000 (open
559
symbols), 2001 (solid symbols), and 2002 (cross-hatched symbols). P-values (determined using a
560
multiple-response permutations procedure) are less than 0.001.
561
562
Figure 2. Non-metric multidimensional scaling (NMS) analysis of (A) bacterial feeding
563
nematodes, (B) fungal and plant feeding nematodes, (C) physical, chemical and biological soil
564
properties, and (D) soil properties and processes related to N cycling. Each data point represents
565
the average of three sampling dates for conventional (triangles), integrated (circles) and organic
566
(squares) systems (n = 12). P-values (determined using a multiple-response permutations
567
procedure) are less than 0.01. The angle and length of vectors indicate the direction and strength
568
of the relationship between axes and nematode groups or soil properties determined using
569
correlation analysis. For example, Heterocephalobus nematodes in panel A are strongly
570
associated with 2 (systems effects) but only slightly so with axis 1. Correlations are provided in
571
Table SX.
572
27
Glover et al.
573
Figure 1.
574
28
Glover et al.
Figure 2.
Axis 2 (71% of variance)
575
A
B
C
D
Axis 1 (21% of variance)
29