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The distribution of organic carbon in soils is outlined, particularly in relation to the return of plant debris to the soil system and the role of soil fauna in these processes.. The man

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CHAPTER 16

Changing Soil Biological Health

in Agroecosystems Julian Park

CONTENTS

Introduction 335

Agroecosystem Sustainability and Soil Health 336

Organic Carbon and Its Distribution in Soils 339

Organic Carbon as an Indicator of Biological Health in Agroecosystems 341

The Quality and Quantity of Crop Debris Returned to the Soil 343

The Growth and Turnover of Plant Roots 343

Cultivation 344

Managing Soil Biological Health 345

Acknowledgments 347

References 347

INTRODUCTION

In an agricultural context, the complexity surrounding the concept of sustainability and the difficulty of moving from consideration of theoretical definitions to practical action currently provide an important issue for researchers (Fresco and Krooneneberg 1992; Park and Seaton 1995; Moffatt et al., 1999) When examining criteria associated with sustainability, there is support for considering the ecological underpinning of production systems that interact with the natural environment (Lowerance, 1990) This is associ-ated with the view that it is desirable for ecosystems to be able to sustain function and thus maintain a given level of productivity into the future

335 0-8493-0904-2/01/$0.00+$.50

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In most agroecosystems, the degree of intervention is usually larger and more frequent than natural disturbance rates, with the primary objective being to maintain productive output Some degradation is both inevitable and acceptable in these systems, with different soil types and climate zones being able to withstand varying levels of intervention (Burke et al., 1995) In ecosystems, such intervention is related to resistance (the ability of a com-munity to avoid displacement in the face of disturbance) and resilience (the speed with which a community returns to its former state after it has been disturbed and displaced) This ability to withstand intervention is similar in nature to the concept of health It is probable that agroecosystems will neces-sarily exist in a less than “full health” state as defined in a natural ecosystem

if they are to remain productive, i.e., a reduction in species diversity, inter-ruption of natural nutrient cycles, and loss of soil structure Further, soil health is increasingly being recognized as an important component of the sustainability of agroecosystems and is an area which is attracting consider-able attention (Pankhurst et al., 1995; Park and Cousins, 1995; Doran et al., 1996; de Bruyn, 1997) If it is assumed that a soil health index (Haberern, 1992) can be agreed, then a key question is how farming practices influence soil health and what mechanisms may lead to improved health

In this chapter, agroecosystem sustainability is discussed in relation to soil health Although there is considerable interest in soil fauna as bioindica-tors, I focus here on soil carbon as a holistic (proxy) measure of soil health The distribution of organic carbon in soils is outlined, particularly in relation

to the return of plant debris to the soil system and the role of soil fauna in these processes The manner in which farming practices affect the amount and distribution of soil organic carbon (organic matter) is discussed before conclusions are drawn about the possibility of altering soil biological health

in productive agroecosystems

AGROECOSYSTEM SUSTAINABILITY AND SOIL HEALTH

Fresco and Kroonenburg (1992) suggest that in order to be sustainable, land use must display a dynamic response to changing ecological and socio-economic conditions In this situation, the maintenance of adaptive capacity within a production system becomes important Soil degradation and erosion

is a serious problem in many parts of the world, both developed and devel-oping (Pimentel et al., 1987) This can often be related to changes in cropping practice or the intensity of cultivation, both of which either directly or indi-rectly change soil structure or properties and thus lead to changes in agro-ecosystem health (Boardman, 1990) An agroagro-ecosystem in a poor state of health will be more vulnerable to certain (inappropriate) farming practices at

a given moment than one in a better state of health For instance, in terms of

an agricultural system, this may mean that there is an increased likelihood of soil erosion, which may reduce the options available for food production at

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some point in the future Assessment frameworks can be envisaged that relate to the concept of sustainability so long as criteria can be put in place to assess possible short- and long-term repercussions of change On the basis of these criteria and knowledge of the current situation, questions need to be asked about the effects of a given change in land use on the options available for food production in the future, and whether this change is following broadly desirable dynamic pathways Park and Seaton (1995) suggest these pathways should maintain and, hopefully, increase the adaptability within a given production system, maintaining a direction which can fulfill both short-term needs (i.e., be economically viable) and long-term objectives (i.e.,

be sustainable) This will require the maintenance of healthy ecosystems There has been substantial debate surrounding the notion of ecosystem health (Schaeffer et al., 1988; Rapport, 1989; Allen and Hoekstra, 1992; Suter, 1993; Rapport et al., 1998) and, in non-agricultural contexts, Constanza (1992) and Rapport (1989) have proposed using ecosystem health as an end point for environmental assessment and management Ecosystem health is defined

by Rapport (1990) as the ability to maintain productivity, to handle stress, and

to recover to equilibrium after perturbation Similar principles can be related

to agricultural systems The need to maintain production (e.g., resistance to disease or inappropriate management) and to recover productive capacity following a larger disturbance (e.g., resilience following flooding or drought) are central facets of desirable agricultural production systems Furthermore,

a measure of the degree of agroecosystem health as a state of a productive unit may be used to monitor sustainable development The success of this approach depends upon finding important variables to measure the state of the system in order to characterize its health from both viability and sustain-ability perspectives

Similar approaches have been utilized to explore the concept of soil health Doran and Parkin (1994) define soil health as the capacity of a soil to function within ecosystem boundaries to sustain biological productivity, maintain environmental quality, and promote plant and animal health Thus,

a measure of soil health may change between soil types and be related to both the present state of the soil and the reserve or potential within the soil to respond to change

In relation to soil biological health, the functional role of soil organisms near the bottom of the food chain, their numbers, mass, and diversity mean that they may provide an indicator of the state of (agro)ecosystems (Pimentel

et al., 1980; Holloway and Stork, 1991; Currie, 1993) Paoletti et al (1991) reviewed the use of soil invertebrates as bioindicators and suggested that

much caution and modesty be associated with their development They point

out that whatever indicators are chosen, they must give a sufficiently clear response to agroecosystem changes, either in terms of abundance or taxo-nomic diversity They further suggest that species level identification is much

more time consuming—if not impossible This reinforces an earlier statement

by Pimentel et al (1980), who suggested the best approach would be to assess

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populations and biomass of major groups of biota without attempting to record data on all individual species present in a given ecosystem However, there is still little consensus on how to assess or monitor major groups of biota Pankhurst et al (1995), working in Australia, researched a wide range

of soil biological properties with respect to different agricultural practices on two long-term field trials They were able to draw conclusions about the responsiveness of differing biological properties to agricultural management and thus their usefulness as biological indicators De Bruyn (1997) reviews the status of macrofauna as indicators of soil health She believes that the challenge for the future is to shift the emphasis of research towards an under-standing of the function of macrofauna in soil processes It has been sug-gested elsewhere (Park and Cousins, 1995) that the use of body-size spectra may enable the development of simple techniques to provide information about the functioning of soil communities, which can be applied rapidly by local researchers who may not necessarily have a high degree of taxonomic training

Doran et al (1996) provide a comprehensive review of soil health and sustainability They believe that the challenge is to develop holistic approaches for assessing soil health that are useful to producers, specialists, and policy makers To explore a more holistic approach, rather than focussing

on the function of certain soil groups in relation to soil biological health, it is suggested here that agroecosystem change be explored via changes in carbon structure and processes associated with its distribution through the soil The distribution and flow of carbon in the form of organic material is of critical importance to soil properties The set of processes creating flows through that structure are gravity, wind, water flow, plant growth, animal movement, and human trade flows Changes in land use activity will alter these flows, giving a measurable change within agroecosystems Regular measurement of carbon in the soil system, together with the processes asso-ciated with its movement, can provide the basis for monitoring strategies, which will enable decisions to be made about whether the process of change

in a given agroecosystem is sustainable Thus, studying the organic carbon structure of soils in parallel with other bioindicators could provide a useful measure of changes in agroecosystems for three reasons:

1 Soil processes are responsive to human intervention Buringh (1984) estimates that on a world basis the soil contains only about three quarters of the organic carbon it did before the spread of civ-ilization, and Doran and Smith (1987) point out that the forests and grasslands of North America declined to between 40 and 60% of their original organic carbon levels following cultivation

2 The processes within the soil are fundamental to plant growth and photosynthesis Perry et al (1989) recognize the importance of the links between the soil and plants that grow on its surface, and how

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this connects with the healthy functioning of the agroecosystem They state that the diversity in the plant community, the microbial community, and the ecosystem as a whole plays a seminal role in buffering against disturbance and in maintaining healthy links between plants and soil

3 The soil itself is the agroecosystem component with the least resilience (Fresco and Kroonenburg, 1992) Thompson (1992) specifically highlights the importance of the soil processes in a short discussion paper on environmental quality objectives He suggests that the first concern must be the protection of the func-tion of the soil—carbon and nutrient cycling and storage, nutrient supply, water supply, filtration and storage, and plant anchorage Further, soil carbon is relatively easy and economic to measure in time and space, responds well to farming practice (although not rapidly), and can be measured without specialist (taxonomic) knowledge Additionally, carbon budgeting and the modeling of carbon and organic matter turnover in soils can provide predictions of the effects of changes in farming practices over time, and a wealth of information already exists on the dynamics and distri-bution of organic matter in soils

ORGANIC CARBON AND ITS DISTRIBUTION IN SOILS

Organic materials act as binding agents within the soil, holding individ-ual particles together A review of the role of organic matter in aggregate sta-bility is provided by Tisdall and Oades (1982) The feces and associated digestive products of many soil organisms aid this stability For instance, residues left by earthworms often increase aggregate stability (in Dutch Polders the aggregate stability was increased by 70% following the introduc-tion of earthworms) Wallwork (1976) suggests that the mucus associated with molluscs (which often move well below the soil surface) is a very good soil-binding agent The same principle is true for all soil animals that add saliva to debris as they ingest it

The bulk density of soils is usually reduced by the presence of organic materials, and soil organisms such as earthworms increase the pore space within the soil (Edwards and Lofty, 1977) Chen and Avnimelech (1986) sug-gest that in soil low in organic matter, soil aeration becomes a limiting factor and cannot be simply offset by ensuring adequate nutrients and water Good soil structure is therefore essential Soil erositivity is decreased as the degree

of well-incorporated organic matter in the soil increases The exceptions are peat-based or organic soils which may contain very high amounts of organic matter (30%) and are therefore susceptible to erosion under certain condi-tions Well-incorporated organic materials add to the stability of soils by

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reducing the direct impact of rain on the soil, increasing aeration, and improving drainage Conversely, compaction of the soil increases water runoff and reduces infiltration Flows of water, at or near the surface, are the precursor of severe rill and gully erosion

This incorporation of organic materials is part of a complex process As plant and root material dies, it collects on the soil surface where it starts to decompose under the action of both sunlight and microorganism activity (Zlotin, 1971) In undisturbed soils, this surface litter provides both food and shelter for a range of sizes of animals Soil animals incorporate organic mate-rial into the soil where further decomposition takes place Decomposition processes have been discussed elsewhere by Edwards et al., 1970; Dickinson and Pugh 1974; Anderson, 1975; Edwards and Lofty, 1977; Persson and Lohm, 1977; Swift et al., 1979; Hole, 1981; and Giller, 1996

Lee (1985) suggests the disintegration, decomposition, and incorporation

of litter results from a combination of solution by percolating rainwater, a minor component of atmospheric oxidation, but most importantly from the

“decomposer industry.” Similar observations were made by Russell (1969) who suggests that soil animals are, in fact, the major and often the sole agents for bringing plant leaf litter into the soil so that it becomes accessible to the soil organisms

The digging activities of the soil invertebrates cause direct infiltration of surface material through their feeding habits Indirect infiltration occurs through the dragging into the soil of organic fragments as water drains through the vertical pores created by invertebrates Earthworms are often cited as major movers and incorporaters of surface debris Edwards et al (1970) commented that earthworms were capable of consuming nearly all of the litter fall from a forest floor (3000 kg ha1) in the absence of other soil ani-mals Although data exist on the disappearance of litter from the soil surface (Van Der Drift, 1963; Edwards et al., 1970; Dickinson and Pugh, 1974; Swift

et al., 1979), rate of litter movement through the profile is less well docu-mented Working with forest soils in the Netherlands, Van Der Drift (1963) recorded litter disappearance rates of up to 4200 kg ha1 in a year Similar

work by Raw (1962) estimated that the earthworm species Lumbricus terrestris

removed about 1.2 t ha1dryweight of leaves from the surface in an English apple orchard

In undisturbed temperate soils, the main invertebrates working below

20 cm will be earthworms, some of which are known to feed on the surface and defecate underground (Lee, 1985) More recent work by Balesdent et al (1990) studying the incorporation of maize debris suggests that 10–20% of the original plant residue carbon ended up below a depth of 30 cm within a 17-year period Although they do not discuss how the carbon arrived in such

a position, it can be speculated that movement was either undertaken by soil animals or by water movement through the channels they make (earthworms

in particular) Other soil-related animals, such as millipedes, centipedes, and

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woodlice, are likely to stay closer to the surface Mesofauna do play a role in the transport of debris, but they are smaller and usually inclined towards predatory or saphrolytic activity within the soil body itself

Mixing and transporting plant debris by the soil fauna often enhances conditions for microbial decay The larger soil animals will commute and break up the detrital material For instance the common earthworm pulls leaf material into its burrows to a depth of 10 cm or more They will often emerge

at night to feed on surface litter or may be forced to the surface when their burrows become waterlogged Persson and Lohm (1977) recognize that many

of the larger soil animals derive their nutrition from the microbial biomass and often ingest plant debris because of the microbes associated with it One

of the benefits of such ingestion is that detrital material is shredded and moved during the process, with the possibility that microbial populations may be dispersed by such activity

It is extremely difficult to estimate the amount of surface material that enters and moves through the soil as a result of water flows It has already been stressed that this flow is enabled by the burrowing and feeding activi-ties of the larger soil animals In undisturbed moist soils (without surface cracking), the activities of soil animals are likely to be the major facilitator in the incorporation of surface debris

ORGANIC CARBON AS AN INDICATOR OF BIOLOGICAL

HEALTH IN AGROECOSYSTEMS

The dynamics of organic carbon have been shown to be of importance in the cycling of nutrients, maintenance of soil structure, prevention of erosion, and diversity of soil organisms (Nye and Greenland, 1960; Allison, 1973; Doran and Smith, 1987) It is evident that organic carbon plays a vital role in many of the processes within the soil and therefore can provide an indicator

of the health of the soil system Agricultural activity affects the amount of organic carbon within the soil, its distribution throughout the profile, and its rate of turnover

Although it cannot be argued that soils of low organic carbon status are

no longer productive, it can be generally assumed that soils very low in organic matter are more susceptible to erosion, suffer from poor structure, and need a constant input of nutrients if production is to be maintained (Chen and Avnimelech, 1986) Mineral soils of higher organic carbon status are usually better structured and are less likely to be eroded

Within agroecosystems, the primary mechanisms by which agriculture influences the dynamics of soil organic matter are by controlling the return of surface debris to the soil, through the crop being grown, and the harvesting method The cropping type and system influences the amount and the qual-ity of plant debris and root material being returned to the soil system Inputs

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Table 16.1 Total Percentage Organic Matter Content of the Top Soil (0 –23cm)

in the Broadbalk Continuous Wheat Experiment 1865 –1987

% organic matter

1865 3.13 1.90 N/A N/A

1914 4.33 1.77 1.92 2.21

1944 4.05 1.80 1.92 2.11

1966 4.35 1.90 2.08 2.11

1987 4.64 1.78 1.94 2.16

N0  0, N1  48, N3  144, kg N per hectare, respectively

FYM  35 tonnes of FYM per hectare,

Figures adapted from %N in top soil by assuming a C:N ratio of 10:1, and carbon to organic matter scaling factor of 1.72.

Adapted from Glendining and Powlson, 1990.

used in the growth of the crop will influence the quantity of crop produced and thus the return of root and plant material Fertilizers and certain chemi-cals can have both a direct effect (by increasing the amount of crop grown) and an indirect effect on the movement and rate of decomposition of organic materials in the soil via their effect on the soil community The effect of fertil-ization can be demonstrated by data from the long-term experiments at Rothamsted Plots that have received higher amounts of nitrogen during the past 150 years have higher levels of soil organic matter in the surface profiles Plots receiving organic fertilization in the form of 35 tonnes of farmyard manure (FYM) directly influence the amount of plant debris entering the soil which explains the large effect its application has had upon soil organic mat-ter (Table 16.1)

Fertilizer and pesticide inputs applied during the growing cycle of a crop

to boost yield are likely to increase the amount of organic matter returned to the soil within the constraints of that particular cropping system However, the effect of that cropping regime, particularly associated cultivation and export of material at harvest, is likely to have an overriding influence on the dynamics of soil organic matter within that particular agroecosystem For instance, the ploughing of virgin land for arable cropping generally results in

a rapid loss of soil organic matter which gradually slows, often reaching a lower, relatively stable state after many years (Lucas et al., 1977; Schlesinger, 1977)

Mann (1986) reviewed the changes in soil carbon storage after cultivation and found all soils high in carbon (5%) lost at least 20% of this following cultivation There are three primary mechanisms associated with this loss: the quality and quantity of crop debris returned to the soil; the growth and turnover of plant roots; and cultivation

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The Quality and Quantity of Crop Debris Returned to the Soil

Campbell et al (1991) suggest that because crop residues are the primary substrata for organic matter replenishment in soils, changes in crops and their management can exert significant influence on soil quality The amount

of plant debris returned to the surface of the soil each year is a function of the crop grown, the inputs used upon it, and the amount of biomass taken away

at the end of the year

The amount of root material and straw returned to the soil depends on how well the crop grows Therefore, high yields of grain will be associated with strong root systems and often more straw and chaff If the straw is baled and taken from the field along with the grain, the organic material returned

to the soil is limited to the chaff and the root material In some crops, the roots (or part thereof) are removed (i.e., carrots, potatoes, etc.), and this can limit the return of organic materials still further However, it is not only the amount of organic matter returned that is important, but also its quality, as this affects the rate of decomposition

The importance of the quality of the residue is highlighted by Wood and Edwards (1992) who consider that crop rotations, owing to the differences in amount and chemical composition of crop residues, may affect soil organic matter concentration and potential mineralization One measure of residue quality is ratio of C:N (carbon to nitrogen) within the plant material, as it is often the availability of nitrogen which controls the rate of decomposition The rate of decomposition can be further retarded by high amounts of lignin Carbon labeling experiments have shown that even substrates such as glu-cose, which decompose rapidly, still contribute to the stable organic materi-als in the soil In fact, a wide range of crops decompose to leave about a third

of their initial carbon in the soil after a period of a year (Paul and Van Veen, 1978) This suggests that although the quality of organic material may gov-ern rates of decomposition processes in the short term, over longer time peri-ods it is the quantity of material returned to the soil which provides a more important determinant of soil carbon content

The Growth and Turnover of Plant Roots

In some agroecosystems the return of surface plant debris is small due to low litterfall, high export, and straw burning In these systems, plant roots provide the major source of organic matter input into the soil (Hansson et al., 1991) Plants vary considerably in rooting pattern and depth, leading to a stratified return of debris Kramer (1983) recognizes that plants have charac-teristic root patterns, although these can be greatly modified by soil condi-tions Water tables can considerably affect the depth of rooting, and in some free draining soils rooting can occur to considerable depths For instance,

maize (Zea mays) roots can often be found at a depth of 2 m, whereas roots of

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lucerne (Medicago sativa) have been recorded at 10 m (Kramer, 1983) Durrant

et al (1973), considering root growth in relation to soil moisture of field crops, found that barley and sugar beet were capable of rooting to well in excess of

1 m, whereas potatoes were extracting water from a depth of 0.8 m

In growing and penetrating through soils, a large amount of organic material is sloughed off into the soil surrounds, and dead root material is returned by both annual and perennial crops Addition of organic matter to the soil by these mechanisms can be considerable as between 50 and 70% of plant production is likely to be belowground growth (Reichle, 1977; Flitter, 1991) The adoption over a period of time of shallow rooting crops can reduce the amount of deep rooting material entering the soil, the consequence of which could be the gradual loss of organic material in deeper soil horizons Roots below the cultivation layer will improve soil structure in this region, where the formation of vertically orientated pores is a necessity for free drainage and further root development (Goss, 1991)

In agricultural terms, perhaps the greatest distinction can be drawn between annual and perennial crops In the latter, roots, root cells, hairs, and tips are constantly being sloughed off and replaced, and this decaying mate-rial supplies a continuum of organic matemate-rials to the soil These perennial systems are not usually cultivated, and this not only allows the plant root sys-tems to become well established but often aids the formation of a healthy soil community

Cultivation

On arable soils, annual cultivation is often used to incorporate surface residues, this operation frequently occurring shortly after harvest Incorporation has two main effects on the dynamics of soil organic carbon: it gives very good mixing of debris and soil leading to favorable conditions for microbial decomposition, but conversely this disturbance can kill a propor-tion of the fauna living in the soil (Madge, 1981)

Microorganisms can multiply rapidly to utilize well-incorporated fresh organic matter, and this is evident in the flush of activity following plough-ing This food supply may be enhanced because cultivation is likely to expose older organic material in the soil to further attack This can lead to rapid min-eralization of carbon and high respiration losses Rapid recovery/reproduc-tion associated with microbial life means that cultivarecovery/reproduc-tion can increase activity, providing a well-mixed food source within the soil microclimate However, populations of larger soil animals may be kept at a permanently suppressed level due to annual cultivation Edwards and Lofty (1982) esti-mated changes in the population of earthworms on ploughed, chisel ploughed, and direct drilled soils They found that on direct drilled soils, the

populations of the deep burrowing Lumbricidae terrestris and Allolobophora longa increased almost 18-fold over the 8 years of the experiment House et al.

(1984) summarize the effects of cultivation on the distribution of soil organic

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