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a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / e c o l e c o n
Soil biota, ecosystem services and land productivity Edmundo Barrios Tropical Soil Biology and Fertility Institute of Centro Internacional de Agricultura Tropical (TSBF-CIAT), Cali, Colombia
AR TIC LE I N FO
ABS TR ACT
Article history:
The soil environment is likely the most complex biological community. Soil organisms are
Received 23 March 2006
extremely diverse and contribute to a wide range of ecosystem services that are essential to the
Received in revised form
sustainable function of natural and managed ecosystems. The soil organism community can
27 February 2007
have direct and indirect impacts on land productivity. Direct impacts are those where specific
Available online 30 April 2007
organisms affect crop yield immediately. Indirect effects include those provided by soil organisms participating in carbon and nutrient cycles, soil structure modification and food web
Keywords:
interactions that generate ecosystem services that ultimately affect productivity. Recognizing
Agriculture
the great biological and functional diversity in the soil and the complexity of ecological
Ecosystem services
interactions it becomes necessary to focus in this paper on soil biota that have a strong linkage
Soil biodiversity
to functions which underpin ‘soil based’ ecosystem services. Selected organisms from different
Soil biological processes
functional groups (i.e. microsymbionts, decomposers, elemental transformers, soil ecosystem engineers, soil-borne pest and diseases, and microregulators) are used to illustrate the linkages of soil biota and ecosystem services essential to life on earth as well as with those associated with the provision of goods and the regulation of ecosystem processes. These services are not only essential to ecosystem function but also a critical resource for the sustainable management of agricultural ecosystems. Research opportunities and gaps related to methodological, experimental and conceptual approaches that may be helpful to address the challenge of linking soil biodiversity and function to the provision of ecosystem services and land productivity are discussed. These include: 1) integration of spatial variability research in soil ecology and a focus on ‘hot spots’ of biological activity, 2) using a selective functional group approach to study soil biota and function, 3) combining new and existing methodological approaches that link selected soil organisms, the temporal and spatial dynamics of their function, and their contribution to the provision of selected ‘soil based' ecosystem services, 4) using understanding about hierarchical relationships to manage soil biota and function in cropping systems, 5) using local knowledge about plants as indicators of soil quality, remote sensing and GIS technologies, and plant-soil biota interactions to help understand the impacts of soil biota at landscape scale, and 6) developing land quality monitoring systems that inform land users about their land's ecosystem service performance, improve capacities to predict and adapt to environmental changes, and support policy and decision-making. © 2007 Elsevier B.V. All rights reserved.
1.
Introduction
In the past century we have seen a dramatic increase in land productivity that has been largely due to the introduction of new crop varieties into farming systems in dryland and irrigated environments with good supplies of fertilizer and pesticides
(Brown et al., 1994). However, in many less endowed areas land productivity has actually been declining in the last decades (Sánchez et al., 1997). Land productivity is defined here as the capacity of agricultural lands to produce biomass on a sustainable long-term basis under the constraints of each agroecological zone (FAO, 2003). High input agriculture that overcomes soil
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constraints to crop productivity through large fertilizer and lime amendments, biocide applications as well as intensive tillage operations, has been one alternative to address this problem. Nevertheless, the low resource use efficiency of these agricultural systems when poorly managed makes economic and environmental costs unacceptably high (Swift and Anderson, 1993). Recent years have shown increasing interest in the development of productive farming systems with a high efficiency of internal resource use and thus lower input requirement and cost. In this context, the importance of soil biota for the improvement of soil fertility and land productivity through biological processes becomes a key component of a strategy towards agricultural sustainability (Woomer and Swift, 1994; Swift et al., 2004; Giller et al., 2005). The majority of ecosystem processes in both natural and managed ecosystems have the soil as the critical and dynamic regulatory center. The soil not only houses a large proportion of the Earth's biodiversity but also provides the physical substrate for most human activities. Although soils have been widely studied and classified in terms of physical and chemical characteristics, knowledge of soil biodiversity and function is far from complete (Swift, 1997; Wall and Virginia, 2000; Swift et al., 2004, Brussaard et al., 2004). This knowledge gap is partly due to the limited recognition that soil biota plays a key role in determining the physical and chemical properties as well as productivity of soils, and partly due to the huge diversity of soil organisms and the difficulties faced for their identification and for the study of their direct linkages to soil function (Brussaard et al., 1997; Lavelle and Spain, 2001; Coleman et al., 2004). The role of soil organisms in high input agroecosystems has received little attention because natural and biologically medi-
ated processes like those regulating soil structure, nutrient supply, and pest and disease control have been largely replaced by human inputs (i.e. soil tillage, fertilizer and pesticide applications) that ultimately depend on non-renewable energy sources. In natural ecosystems, the internal regulation of function is largely a result of plant biodiversity that influences the magnitude and temporal distribution of C and nutrient flows; however, this form of control is increasingly lost through agricultural intensification (Swift and Anderson, 1993). Therefore, the sustainability of high input agroecosystems could be compromised because of their lower biological capacity for self-regulation in response to environmental change and greater dependence on external and market-related factors (Swift et al., 2004). The consensus about societal demands for agricultural sustainability and biodiversity conservation reached in the past decade (UNCED, 1992) has catalyzed the current shift towards sustainable land use, particularly in agriculture. Additionally, the growing recognition of the world's biota as the life support system for our planet has also led to renewed interest in soil biodiversity as a resource to study in terms of the biota's functional roles and for sensible management to optimize their contribution to ecosystem services (Costanza et al., 1997; Swift et al., 2004). Ecosystem services are ‘the benefits people obtain from ecosystems’ as defined by the Millenium Ecosystem Assessment (MA, 2003). The purpose of this paper is to explore and discuss the direct and indirect impacts of soil biota on key ecosystem services and land productivity in agricultural landscapes and illustrate with case studies the untapped potential that can result from studying, understanding, and wisely managing the soil biota.
Fig. 1 – Size classification of soil organisms according to body width (from Swift et al., 1979).
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Table 1 – Estimated number of species of plants and of soil organisms organized according to body size (modified from Wall et al., 2001)
a
Estimates for Vascular plants (UNEP, 1995).
2.
Soil biota inside out
The soil environment hosts a complex and diverse biological community likely because of its extremely high physical and chemical heterogeneity at small scales, microclimatic characteristics, and phenologies of organisms that promote the development and maintenance of an extremely large number of niches (Tiedje et al., 2001; Ettema and Wardle, 2002). Soil organisms have been classified on the basis of body width into microflora (1–100 μm, e.g. bacteria, fungi), microfauna (5– 120 μm, e.g. protozoa, nematodes), mesofauna (80 μm–2 mm, e.g. collembola, acari) and macrofauna (500 μm–50 mm, e.g. earthworms, termites) (Fig. 1, Swift et al., 1979; Table 1, Wall et al., 2001). One trend from Table 1 is that inventories of soil organisms have been considerably limited compared to those of above-ground organisms such as vascular plants. Another trend is that soil organisms of greater size (i.e. macrofauna) have received far greater attention than smaller soil organisms despite the greater diversity of the latter. For example, while millions of bacteria and fungi are often found in fertile surface soils (Tiedje et al., 2001), only about 0.1% of microbial taxa have been cultured and their metabolic role understood (Torsvik et al., 1994). These trends, however, are starting to change as a result of the increasing use of molecular techniques to study soil microbial diversity and function (Lynch et al., 2004). Nonetheless, the difficulty of studying soil biodiversity and the need to identify common methodologies with global application continues to be one of the greatest challenges in soil science (Giller et al., 2005). Soil biota must be selectively studied because of their high diversity and wide distribution in the complex and heterogeneous soil matrix at scales ranging from microns to meters. This has made difficult the identification of a single method that simultaneously provides information about all components of soil biota. For instance, functional aspects of soil biota have been studied by focusing on ‘hot spots’ of biological activity such as soil microbial habitats associated with soil organic matter (SOM) fractions (e.g. Cambardella and Elliot, 1994; Barrios et al., 1996a,b, 1997; Phiri et al., 2001; Blackwood
and Paul, 2003) and soil aggregates of different diameters (Kandeler et al., 1999; Sessitsch et al., 2001; Mummey et al., 2006). Beare et al. (1995) also identified areas of concentrated biological activity, namely the detritusphere (zone of recognizable plant and animal detritus undergoing decay), the drilosphere (earthworm burrows lined with mucilages and other C and nutrient rich excretions), the porosphere (water films and channels between aggregates), the aggregatusphere (interstices within macroaggregates and between microaggregates) and the rhizosphere (zone of soil directly influenced by the roots and their exudates). Other hierarchical approaches have also been proposed to study soil biota that include a focus on the biogenic structures they produce and other ‘functional domains’ (Lavelle and Spain, 2001), and more recently Swift et al. (2004) and Decaens et al. (2006) have proposed an organization based on the ecosystem services provided. Soil food web analysis has been a useful approach for understanding nutrient cycling and energy flows in the soil community as well as for drawing relationships between soil food chain dynamics and agroecosystem stability (Susilo et al., 2004; Van der Putten et al., 2004). Soil macrofauna break dead organic matter into smaller pieces and facilitate decomposition by soil bacteria and fungi that start the mineralization of organic nutrient forms into inorganic nutrients essential for plant growth. Mineralization continues with the action of organisms like protozoa and nematodes that feed on bacteria and fungi, while first and higher order carnivores eat these in turn. All of these food web or trophic interactions, critical for energy and nutrient flow through the ecosystem, were graphically represented in a seminal paper by Hunt et al. (1987) and shown here as Fig. 2. More recently, De Ruiter et al. (1995) have shown that stability of the soil ecosystem is closely linked to the relative abundance of the different functional groups of organisms (i.e. soil food web structure). Nevertheless, the question of how many species are needed to sustain the ecosystem processes that are the basis for ecosystem service provision remains an issue of much debate. The limited application of food web approaches to environmental issues has been largely a result of the little existing knowledge
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Fig. 2 – Graphic representation of a detrital food web in a shortgrass prairie (from Hunt et al., 1987).
about the spatial and temporal variability of soil biodiversity and function (De Ruiter et al., 2005). Soil biodiversity is best considered by focusing on the groups of soil organisms that play major roles in ecosystem functioning when exploring links with provision of ecosystem services. Activity measurements provide a better understanding of soil biological function than do counting soil organisms or measuring biomass (Brussaard et al., 2004; Coleman et al., 2004). However, there is increasing experimental evidence that highlights the complexity of relationships between diversity and function. Given the multifunctional nature of many soil organisms it is increasingly apparent that abundance and diversity of different species are relatively less relevant than the functional attributes of soil community members (Ritz et al., 2003; Hooper et al., 2005). This realization has led to the identification of sets of species or functional groups that are responsible for essential ecosystem processes (Wall and Moore, 1999; Bloem et al., 2003; Swift et al., 2004). Key functional groups of soil biota and the ecosystem processes they influence include: i) microsymbionts (e.g. N-fixing organisms, mycorrhiza), ii) decomposers (e.g. cellulose and lignin degraders), iii) elemental transformers (e.g. nitrifiers, denitrifiers), iv) soil ecosystem engineers (e.g. earthworms, termites), v) soil-borne pest and diseases (e.g. white grubs, plant-parasitic nematodes, root-rots) and vi) microregulators (e.g. grazers, predators, parasites).
3.
Soil biota and ecosystem services
Soil organisms are an integral part of the soil and influence ecosystem processes that contribute to the provision of a wide
range of essential ecosystem services. Recent efforts to address the complexity of this topic have proposed research frameworks, approaches, and questions to examine the linkages between biodiversity, ecosystem function and the provision of ecosystem services in both natural and managed landscapes (MA, 2003; Swift et al., 2004; Bulte et al., 2005; Giller et al., 2005; Jackson et al., 2005; MA, 2005). According to the Millennium Ecosystem Assessment (MA, 2003), ecosystem services can be classified into those associated with the provision of goods (e.g., food, fiber, fuel, fresh water), those that support life on the planet (e.g., soil formation, nutrient cycling, flood control, pollination), those derived from benefits of regulation of ecosystem processes (e.g., climate regulation, disease control, detoxification) and those cultural services that are not associated with material benefits (e.g., recreation, aesthetic and cultural uses). Soils contribute to all four different dimensions of ecosystem services, but the focus of this review will be on key ecosystem services in agricultural landscapes linked to the roles of life support and of regulation of ecosystem processes.
3.1.
Life support role
3.1.1.
Nutrient cycling
The cycling of nutrients is a critical ecosystem function that is essential to life on earth. Positive direct impacts of microsymbionts on crop yield due to increases in plant available nutrients, especially nitrogen (N) through biological nitrogen fixation (BNF) by soil bacteria (e.g. Rhizobium) and phosphorus (P) through arbuscular mycorrhizal fungi (AMF), have been especially well documented (Giller, 2001; Smith and Read, 1997). Decomposition and elemental
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transformation have also received great attention as a result of their essential role in biogeochemical cycles (Swift et al., 1979; Coleman et al., 2004).
3.1.1.1. Nitrogen fixing organisms. Nitrogen is essential for plant growth and often an important constraint to agricultural productivity. A basic prerequisite for sustainable agricultural systems is maintaining an overall nutrient balance to ensure that outputs of nutrients as agricultural products and unwanted losses are compensated by nutrient inputs. When N is the limiting soil nutrient and access to fertilizers constraints its usage, as in many parts of the tropical world, BNF can play an important role in providing N inputs to the cropping system budget. BNF can contribute to productivity in at least three ways: i) where the fixed N goes directly into the harvested product (i.e. grain, leaves or fuelwood); ii) where the fixed N goes into fodder used in animal production, and iii) by contributing to the maintenance and restoration of soil fertility (Giller, 2001). Several organisms present in agricultural systems can fix N at different rates and even within the same BNF system differences can be large, as shown in Fig. 3. While estimates of symbiotic BNF can be as high as 400 kg N ha− 1yr− 1, average associative BNF is about 10-fold lower and free-living BNF by heterotrophs about 100-fold lower. For example, in lowland rice systems, the symbiosis of the N-fixing cyanobacterium Anabaena and the floating aquatic fern Azolla can contribute as much as 76 kg N ha− 1yr− 1, with at least 70% of this N derived from the atmosphere through BNF, and thus account for a considerable proportion of the rice N requirements (Ladha and Reddy, 2003). Considerable non-symbiotic BNF has also been reported for other non-legumes (Baldani et al., 1997), as well as for endophytic bacteria growing in stems and leaves of sugarcane (Boddey et al., 2003). The Rhizobium-legume symbiosis remains, however, the most important BNF source in agriculture owing to its widespread use. In temperate climates, the total amount of legume fixed-N in mixed stands of clover (Trifolium spp.) and tall fescue (Festuca arundinacea) can range as high as 300–390 kg N ha− 1yr− 1 (Mallarino et al., 1990a), with as much as 60% of grass N
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provided by the legume in the second year of sward establishment (Mallarino et al., 1990b). Similar magnitudes of BNF have been found by Ledgard (1991) in grazed pasture swards of white clover (Trifolium repens) and rye grass (Lollium perenne). Recent studies in the tropics have shown large yield increases in common bean (Phaseolus vulgaris) as a result of selecting native Rhizobium strains with high N fixation rates, good competitive ability, and tolerance to high soil temperatures, soil acidity, and water stress (Hungria et al., 2003). Brazilian bean cultivars in nitrogen-limited soils inoculated with best performing native strain PRF81 produced about 2500 kg ha− 1 which corresponds to more than four times the national bean production average. This example shows that exploring the variability in genetic capacity to fix N even within closely related organisms can be of benefit to the ecosystem service of N supply.
3.1.1.2. Arbuscular mycorrhizal fungi (AMF). Phosphorus deficiency is also a widespread nutrient constraint to crop production, but as for N fertilizer, P fertilizer applications are also often not a viable option in many parts of the world (Sánchez et al., 1997). Several alternatives have been proposed for sustainable P management in agriculture that include: i) increased P acquisition by crop exploration of a greater soil volume, ii) the development of more P efficient germplasm, and iii) improved soil management practices that minimize P flows that limit availability (i.e. P fixation reactions) and that maximize P flows through dynamic pools that contribute to increased soil P availability (Phiri et al., 2001; Rao et al., 2004). Soil biota can directly affect P acquisition through mycorrhiza, i.e. the symbiosis between specific soil-borne fungi and roots of higher plants. There are two main types of mycorrhiza: endomycorrhiza and ectomycorrhiza (Smith and Read, 1997). Endomycorrhiza, commonly known as arbuscular mycorrhizal fungi or AMF, are especially important for cropping systems because of their wide geographic and taxonomic distribution, and also because they are commonly found under natural conditions in association with almost all tropical and subtropical crops. A key mechanism by which AMF increase P acquisition by plants is through the
Fig. 3 – Type, energy source and fixation capabilities of biological N2 fixation systems in soils (modified from Marshner, 1995).
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exploration of a large soil volume by hyphal networks (Jakobsen et al., 1992). Symbiotic efficiency studies with sorghum and three different AMF species indicate that Glomus macrocarpum shows twice as much percent root colonization and ten times greater hyphal lengths, compared to G. intraradices and G. fasciculatum, leading to more than five times greater P uptake by sorghum plants (Marshner, 1995). This example highlights that dramatic differences in P uptake, and thus the ecosystem service of P supply, can be found among closely related AMF species of the same genus. Conservative estimates would suggest that comparisons among AMF genera would show differences in symbiotic efficiency that are at least equal to those found among species of the same genus. Increased nutrient acquisition by native plants and crops, however, is not restricted to P, as greater acquisition of soil mineral N (e.g. ammonium) and other soil nutrients like potassium, calcium and magnesium have also been improved when plants are mycorrhizal (George et al., 1992). Improved nutrition results in enhanced relative growth rate of plants by the AMF symbiosis with direct positive impact on crop productivity. However, in some cases the net cost of the symbiosis can exceed the net benefits and AMF can become parasitic and compromise productivity (Johnson et al., 1997). Indirect effects of AMF on soil P availability have been shown through the activity enhancement of phosphate-solubilizing rhizobacteria (Barea et al., 1997). The microbially solubilized phosphorus is taken up by the AMF through a synergistic interaction of particular importance to plant productivity in soils where phosphorus is the limiting nutrient. Furthermore, the significantly greater plant growth and survival rate of AMF-colonized plants used to rehabilitate degraded lands has made AMF inoculation a key entry point to restoring land productivity (Requena et al., 2001; Allen et al., 2005).
3.1.1.3. Decomposers and elemental transformers. The decomposition of organic materials into simpler molecules is one of the most important ecosystem services performed by soil organisms as it represents the catabolic complement of photosynthesis. Decomposition involves physical fragmentation, chemical degradation, and leaching of organic substrates. The physical fragmentation of detritus during feeding by small invertebrates increases its surface area and thus facilitates colonization and invasion by microbes and their enzymatic action, resulting in leaching of soluble organic compounds. This process is followed by chemical degradation via enzymes produced by bacteria, fungi, protozoa, and invertebrates. Finally, soluble organic and inorganic compounds leach from dead organic matter and detritus (Swift et al., 1979; Coleman et al., 2004). Other authors simply define decomposition as the mineralization of carbon; 90% is carried out by microorganisms such as bacteria and fungi greatly facilitated by soil meso and macrofauna that fragment residues and disperse microbial propagules (Brussaard et al., 1997). Soil macrofauna, especially earthworms, have important impacts on SOM dynamics and nutrient cycling largely determined by their density and behavior (Lavelle et al., 1997). Epigeic species such as Dendrobaena octaedra live in the litter layer, primarily feed on leaf litter, contribute to mixing of plant residues on the mineral top soil, and are good compost-
makers. Anecic species such as Lumbricus terrestris feed on surface litter, build and live in large gallery networks, translocate large amounts of leaf litter into the soil profile, and produce casts on the soil surface that contribute to intimate mixing of soil and organic particles. Endogeic species such as Pontoscolex corethrurus live and feed within the soil on organic substrates of different qualities like roots and SOM and produce casts and burrows that are important sites of microbial and plant root activity as well as organic matter decomposition (Lavelle and Spain, 2001; Coleman et al., 2004). From an applied point of view, the adaptive management of soil biodiversity can have extraordinary impacts on crop productivity. Studies by Senapati et al. (1999) have shown dramatic increases in tea yields (239%) and profitability (US$ 5500 ha− 1) that have been possible through the restoration of soil fertility by trenching of tea prunings, organic materials, and earthworms between tea rows (Fig. 4). Field trials have shown that inoculation of agricultural soils with assemblages of earthworms with different functional types can simultaneously influence a wider array of soil processes than single species inoculation. This is because the cumulative impacts of vertical and horizontal burrows, surface casting, residue incorporation, and acceleration of plant residue decomposition can lead to improved land productivity even in intensive agriculture production systems (Senapati et al., 1999). The impacts of soil biota on productivity, however, are not unidirectional but rather part of a feedback cycle because cropping systems also influence the soil biota. A good example of this is the conversion of conventional tillage to no-tillage agricultural systems where food webs change from being predominating bacteria-driven to predominantly fungi-driven (Beare et al., 1992, 1993; Frey et al., 1999). This change in the composition of microbial communities can have large impacts on soil function by affecting efficiency of nutrient cycling processes. For example, the activity of nitrifier and denitrifier microorganisms in the soil is responsible for large N losses in both natural and managed ecosystems (Dalal et al., 2003). This is because when soil nitrate produced by nitrifiers is not used by plants it is mainly subjected to leaching losses down the soil profile or to gaseous losses mediated by denitrifiers. Nitrogen losses are of particular significance in agricultural lands because they can reduce crop productivity and contaminate ground-and surface-waters. Nitrous oxide gaseous losses have
Fig. 4 – Tea production with and without organic matter additions and earthworm inoculation in Tamil Nadu, India (modified from Senapati et al., 1999).
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received special attention because of their important contribution to global warming potential (Robertson et al., 2000).
3.2.
Regulation of ecosystem processes
3.2.1.
Soil structure modification
Soil structure can be defined as the arrangement of sand, silt and clay particles as well as SOM into aggregates of different size by organic and inorganic agents. The size, quantity and stability of soil aggregates reflect a balance between aggregate forming factors (i.e. organic matter amendments, soil microorganisms and fauna) and those that disrupt them (i.e. bioturbation, cultivation) (Six et al., 2002). The role of soil organisms in soil structure modification has been longrecognized by farmers, but it was only about 25 years ago when the impact of soil organisms on aggregate formation was first conceptualized in the form of the hierarchical model of soil aggregation (Tisdal and Oades, 1982). This model proposes that microaggregates, already stabilized by persistent organic binding agents of bacterial origin, are bound together by temporary (roots and fungal hyphae) and transient (plant and microbial polysaccharides) binding agents to form macroaggregates. The concept of microaggregate formation inside macroaggregates was later proposed by Oades (1984) and further supported by Angers et al. (1997) and several other studies.
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Six et al. (1998) further proposed the ‘aggregate dynamic model’ that directly links aggregate formation and breakdown in soils to the turnover of particulate organic matter (POM) as mediated by microbial and macrofauna activity (Fig. 5). This model proposes that several biological processes in the soil lead to the formation of “biological macroaggregates” and their stabilization as part of soil structure through the activity of fungi and bacteria, plant roots and macrofauna (e.g. earthworms) (Six et al., 2002). Soil macroaggregate breakdown increases with age because the action of binding agents is progressively disrupted. However, microaggregates remain stable to disruptive forces and thus become potential building blocks during the formation of new soil macroaggregates. Recent studies show a strong relationship between glomalin, an AMF produced glycoprotein, and water stable aggregation in different soil types (Wright and Upadhyaya, 1996, 1998). The contribution of AM fungal hyphae to the formation and stabilization of soil structure is related to several factors that include soil characteristics, vegetation type, management practices, and the inherent characteristics of the fungus (Miller and Jastrow, 2000). Studies by Rillig et al. (2002) comparing different functional groups of plants (i.e. grasses, legumes, forbs) showed that direct effect of glomalin was much stronger than that of AMF hyphae as a mechanism of soil aggregate stabilization. The major contributions to soil quality and land productivity through habitat engineering,
Fig. 5 – Biological mechanisms of soil aggregate formation and turnover (modified from Six et al., 2002).
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influence on plant physiology and soil ecological interactions place AMF as a “keystone mutualist” as highlighted by Miller and Kling (2000) and Rillig (2004). Soil macrofauna also play an important role in soil structure modification through bioturbation and the production of biogenic structures (Brussaard et al., 1997; Lavelle and Spain, 2001). Ants, termites, and earthworms modify their surrounding environment and thus affect soil water and nutrient dynamics through their impact on other soil organisms (Lavelle et al., 1997). For example, indirect management of termites through the application of organic mulch has allowed the recuperation of surface sealed soils in Burkina Faso (Mando et al., 1996). Soil crusting is considered one important form of soil degradation that limits land productivity because it considerably reduces soil water infiltration and root growth. Further studies by Mando and Miedema (1997) showed that the strategic application of cow manure and straw to crusted soil surfaces, just before the onset of rains and during termite foraging periods, stimulated the burrowing and feeding activities of termites, which in turn increased soil macroporosity and resulted in the restoration of crusted Sahelian soils. The importance of having a suitable balance between soil organisms producing biogenic structures and bioturbators that break them up has been highlighted by Blanchart et al. (1999) and Barros et al. (2001). It has been shown that the great dominance of the soil-compacting species in parts of Amazonia (e.g. Pontoscolex corethrurus) can lead to pasture degradation as a result of surface crusts that limit infiltration of water in the soil (Chauvel et al., 1999).
3.2.2.
Pest and disease control
Soil-borne pest and diseases cause enormous global annual crop losses. A healthy soil community has a diverse food web that keeps pests and diseases under control through competition, predation, and parasitism (Susilo et al., 2004). There is a strong relationship between soil biota, soil fertility and plant health (Altieri and Nichols, 2003). Crops growing in impoverished soils are increasingly weaker as a result of poor nutrition and thus more susceptible to pest and disease attacks. For example, maize infestation with the parasitic weed Striga sp. in N deficient African soils was significantly reduced following N-fixing tree legumes used as planted fallows that increased soil N availability through BNF and decomposition (Barrios et al., 1998). Further, in northern Cameroon, maize and sorghum inoculated with AMF (Glomus clarum and Gigaspora margarita) and grown in Striga hermonthica infested soils was effective in reducing S. hermonthica emergence by 30–50% and biomass by 40%–63% (Lendzemo et al., 2005). This was also largely because improved nutrition leads to healthy plants that are better able to resist or tolerate pest and diseases. There is general consensus that a diverse soil community will not only help prevent losses due to soil-borne pests and diseases but also promote other key biological functions of the soil (Wall and Virginia, 2000). Three groups of soil organisms–white grubs, plant-parasitic nematodes, and root-rots–represent especially relevant examples of soil-borne plant health problems in agriculture. White grubs are C-shaped larvae of a large group of beetles called scarabs that are able to reach damaging high population densities in agricultural environments by feeding on a wide
range of food resources (Potter, 1998). White grubs and other soil dwelling pests have proven difficult to control because they have evolved strong defense mechanisms to survive in the soil environment where they are exposed to a wide range of microbes and their toxins (Jackson, 2003). Biological control of the New Zealand grass grub Costelytra zealandica, which causes significant economic damage in pastures because it feeds on the roots of grasses and clover, has been particularly effective by entomopathogenic bacteria Serratia entomophila (Jackson et al., 1992; Hurst et al., 2004) because it is highly host specific. The entomopathogenic fungi Beauveria brongniartii and Metarhizium anisopliae have also been effective for controlling white grubs (Keller et al., 1997; Bridge et al., 1997). The provision of the ecosystem service of biological control by these three species has been sufficiently consistent and commercial products have been patented. Plant-parasitic nematodes are microscopic soil worms that represent a major problem in agricultural soils because they reduce the yield and quality of many crops and thus cause great economic losses (Barker, 2003). The root-knot nematodes of the genus Meloidogyne are considered most important because they are widely spread, attacking most major crops as well as many non-crop plant species. Root-lesion nematodes of the genus Pratylenchus are also of economic importance and facilitate the action of other root pathogens (Barker, 2003). Nematodes have a variety of microbial antagonists that include nematophagous fungi, endophytic fungi, actinomycetes, and bacteria (Dong and Zhang, 2006). Nematophagous fungi with greatest biocontrol capacity include nematode-trapping fungi (e.g., Arthrobotrys irregularis) and fungi that parasitize eggs and females (e.g., Paecilomyces lilacinus) (Dong and Zhang, 2006). Arbuscular mycorrhizal fungi of the genus Glomus have been shown to significantly reduce the severity of root galling and reproduction of root-knot nematode Melidogyne incognita resulting from inoculation with G. fasciculatum in tomato (Bagyaraj et al., 1979), with G. mosseae in banana (Jaizme-Vega et al., 1997), and with G. intraradices, G. mosseae or G. viscosum in olive planting stocks (Castillo et al., 2006). The actinomycete Streptomyces avermitilis and bacteria Burkholderia cepacia are also effective nematode antagonists, and in addition to the nemathophagous fungi mentioned earlier, have been patented as biocontrol agents and commercialized (Dong and Zhang, 2006). Root-rot fungi also cause large economic losses worldwide (Haas and Défago, 2005). Plant-beneficial rhizosphere bacteria that have shown great potential for protecting plant roots from fungal-induced diseases include the fluorescent Pseudomonas spp (Haas and Keel, 2003). The biocontrol abilities of such strains depend on rapid root colonization, production of antifungal antibiotics, induction of systemic resistance in the plant, or specific interference with fungal pathogenicity factors (Haas and Défago, 2005). Strains of Pseudomonas fluorescens have been shown to suppress take-all disease of wheat produced by Gaeumannomyces graminis var. tritici and black root-rot of tobacco generated by Thielaviopsis basicola, as well as induced root diseases of cucumber caused by Pythium ultimum (Laville et al., 1992) and damping-off disease in sugar beet caused by Rhizoctonia solani and P. ultimum (Andersen et al., 2003). Several studies have also shown that plants colonized by AMF show reduced soil-borne pathogens incidence and severity (Azcon-Aguilar and Barea, 1996). For
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example one recent study with mung bean plants colonized by AM fungi Glomus coronatum showed reduced colonization of roots by Rhizoctonia sp (Kasiamdari et al., 2002). Several mechanisms have been proposed to explain increased resistance or tolerance to soil-borne pathogens that include: i) increased nutrient uptake as a result of AMF colonization results in more vigorous plants that are able to resist or tolerate roots diseases, ii) competitive exclusion of pathogens by AMF occupancy of colonization sites, iii) changes in root exudation as a result of colonization and enhanced P uptake may inhibit pathogen spore germination and infection and/or promote microbial shifts that could influence plant health, and iv) lignification of roots cells that limit penetration of pathogens to plant roots (Azcon-Aguilar and Barea, 1996). These examples highlight substantial opportunities for biological control of soil-borne pest and diseases.
4.
Research gaps and opportunities
4.1.
Soil biota ‘hot spots’ and ecosystem service providers
The general consensus that soil spatial heterogeneity is largely responsible for soil biodiversity highlights the importance of integrating spatial variability research in soil ecology for better understanding the links between soil biota structure and function (Tiedje et al., 2001, Ettema and Wardle, 2002). Several studies show that soil biota distribution in space and time is not at random or homogeneous but rather concentrated in ‘hot-spots’ of activity that are mostly associated with the availability of C substrates (Beare et al., 1995; Lavelle et al., 1997). This suggests that future studies linking soil biota to soil processes and ecosystem services should increasingly focus on ‘hot spots’ of activity by soil biota that include the
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rhizosphere and the AMF hyphosphere, biogenic structures (i.e. soil aggregates), soil C pools (e.g. POM), and organic detritus. The general agreement that biological processes are not randomly distributed in soil is consistent with conceptual and experimental approaches that concentrate where a large proportion of the biological activity is taking place. Ecological research to date has produced evidence supporting the general relationship between biodiversity and ecosystem functioning; however, these studies have been largely short-term, small-scale, and with limited coverage of trophic levels (Hooper et al., 2005; Bulte et al., 2005). Considerable uncertainty exists about extrapolation of results to the landscape scale (Loreau et al., 2001) and there is a need to identify ways to apply existing knowledge about soil biodiversity and function to real changes in biodiversity occurring in agricultural landscapes (Jackson et al., 2005). Designing experiments with larger plots, involving a greater range of trophic levels, for long-term studies would be one way to address this issue. An alternative approach, however, may consider utilizing data on patterns of soil biodiversity and function in relation to gradients of physical factors at larger scales and across existing time-series (Bulte et al., 2005). The use of agricultural intensification gradients as the basis of landscape experimental design is consistent with the latter approach and has been proposed by Giller et al. (1997) to gain greater understanding of soil biodiversity and how it influences ecosystem functioning and the provision of ecosystem services. Plant-soil biota interactions have received increasing attention to help understand the impacts of soil biota at larger scales (Wardle et al., 2004). Given the difficulty of studying soil biota in agricultural landscapes, greater knowledge about linkages between plant and soil biodiversities is of particular importance because spatial information about the above-ground component obtained through remote sensing and GIS technologies could
Fig. 6 – Research approach for the selective study of key functional groups of soil biota linked to soil processes that underpin ‘soil based’ ecosystem services.
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Fig. 7 – Key functional groups of soil biota, soil processes they influence and ecosystem services they provide in agricultural landscapes.
lead to inferences about the below-ground component (Wall and Virginia, 2000). Further guidance and focus (Fig. 6) could also be provided by taking advantage of existing local knowledge about plants used as indicators of soil quality by farmers and others in agricultural landscapes (Barrios and Trejo, 2003; Barrios et al., 2006). This is consistent with the notion that the nature of the plant community plays a major role in ecosystem service provision sustainability (Swift et al., 2004) and that plant species identity, rather than diversity, may be a key driver of soil function (Diaz and Cabido, 2001; Wardle et al., 2006).
4.2.
Soil functional diversity and ecosystem services
There is growing experimental evidence highlighting the complexity of relationships between soil biodiversity and function. The observation that species richness in the soil is considerably greater than functional diversity has led to the notion of functional redundancy assumed for many soil species (Andren et al., 1995). This issue raises two questions: does it matter if one species disappears, and if so, could another species predictably replace its function. While functional redundancy ensures the stability of an essential ecosystem function like nutrient cycling, it has been also perceived as a limitation to study the link between soil community structure and decomposition processes as there are so many organisms involved (Swift and Anderson, 1993). Nevertheless, there are distinct examples where changes in diversity have compromised the provision of ecosystem services such as the biological control of pest and diseases or the maintenance of soil structure (Swift et al., 2004). Therefore, the question of potential thresholds of species richness required for sustained function and the provision of ecosystem services remains an important issue to be explored. The historical separate existence of two research approaches in soil biology (organismal vs. functional) has contributed to the limited progress in understanding soil biota and function. The existing inability to conduct species removal experiments under field conditions has also limited greater understanding of soil functional diversity (Coleman et al., 2004). Nevertheless,
despite their limitations in addressing the full complexity of soil community interactions and the multifunctional nature of many soil organisms, microcosm and modeling approaches have provided useful information to stimulate further hypothesis testing. The pooling of species into functional groups with “keystone species” and “redundant species” can be considered a conceptual effort to simplify and get an operational handle on the great complexity of soil community interactions. For instance, while modeling the effects of soil biodiversity loss on ecosystem function, by consecutive single deletions from a simple soil community composed of 15 functional groups Hunt and Wall (2002) found that only deletions of bacteria and saprophytic fungi led to the extinction of other groups. This suggested that no other single functional group studied had significant effects on ecosystem function. Conversely, other studies with similar food webs had shown that predatory mites and nematodes had a disproportionately high effect on ecosystem function in relation to their low biomass (Moore and De Ruiter, 2000). These apparently contradictory results highlight the great complexity of soil community interactions as well as the still incomplete databases and limited experimental approaches currently available to address such complexity. Therefore, at present a selective functional group approach (Fig. 7) rather than an exhaustive approach is likely to be a more practical and effective way to study the linkages between potentially manageable soil biota and tangible functions that underpin ‘soil based’ ecosystem services that can increase agricultural sustainability (Swift et al., 2004; Giller et al., 2005; this paper). Knowledge of hierarchical relationships is also useful to guide potential ecosystem management actions directed to conserve or improve the provision of ecosystem services. Integration of new and existing methodological approaches that link identity and function of soil organisms, experimental approaches under field conditions, and conceptual approaches that look at soil communities and processes at different scales would help develop greater understanding on linkages between soil functional diversity and the provision of ecosystem services. The strategic use of PCR-based fingerprinting
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Fig. 8 – Potential entry points for biological management of beneficial and harmful soil organisms through cropping system and organic matter inputs (from Swift, 1998). techniques for organisms detection, DNA sequencing to identify all genes present in species, and microarray technologies to detect patterns of gene expression (Tiedje et al., 2001; Wu et al., 2004; Cole et al., 2005), of stable isotopes (13C and 15N) that allow close and detailed monitoring of soil biological processes and food web interactions (Radajewski et al., 2000; Schmidt et al., 2004), of Near Infrared Reflectance Spectrometry —NIRS that allows both attribution of biogenic structures to specific soil organisms as well as rapid and reliable characterization of soil properties across large areas (Shepherd and Walsh, 2002; Hedde et al., 2005; Velasquez et al., 2005), together with GIS technologies that allow integration of multiple spatial datasets (i.e. vegetation, soil biological, soil chemical and physical parameters, etc.) are among useful methodological approaches to be combined in future research for a fuller understanding of the linkages between soil biodiversity and function at different spatial and temporal scales. Furthermore, new tools in statistical analysis and bioinformatics are needed to handle the very large amounts of data obtained through these integrative multidimensional studies.
4.3.
Hierarchical management of soil biota
The management of soil biota for sustainable agriculture requires a thorough understanding of ecosystem processes linked to ‘soil based’ ecosystem services and of the scale at which each member of the soil biota makes its exclusive contribution (Giller et al., 2005). Swift (1998) conceptualized the structure of agricultural systems as comprised of three levels at which soil biota can be managed. These management levels occur in a nested hierarchy where the cropping system level is at the top of the hierarchy followed by the soil management level and finally the keystone soil biota level (Fig. 8). At the cropping system level, the choice of plants and their arrangement in space and time or their genetic make-up greatly influence the type and “quality” of organic resources produced and of symbiotic relationships as well as types of
possible rhizospheres. Soil management practices like tillage operations (e.g. conventional vs. no-tillage systems), the addition of organic inputs of different qualities (that determine their residence time and patterns of nutrient release and potential secondary compounds), and mineral fertilizers and other amendments would also have important effects on soil biodiversity and function. Finally, at the keystone biota level, beneficial soil organisms with special capabilities in nutrient supply, soil structure modification, and biological control can be added to the agroecosystems to improve their performance in the provision of ‘soil based’ ecosystem services. The partial or complete impairment of the ecosystem service of biological control of pest and diseases is probably the most evident to farmers because of the dramatically visual impact that pest and diseases can have on crops and productivity. Agriculture can induce changes in the soil environment, generating preferential advantage to some organisms (i.e. limiting the number of natural predators) and thereby favor their growth to levels at which they become pests. Understanding the soil fertility basis and critical values responsible for a decrease in natural resistance to pests and diseases would allow the development of integrated and resource use efficient soil fertility management options that could reduce pest and disease problems. Soil management practices involving organic residue management such as crop rotations, green manures, and improved fallow systems influence the soil community through changes in soil organic matter quantity and quality (Swift et al., 2004; Wardle et al., 2004). As soil organic matter influences soil structure, soil nutrient availability, soil water holding capacity, and cation exchange capacity it can be used as a management tool to favor greater soil heterogeneity and more diverse soil communities that are associated with the natural regulation of pests and diseases. Further research is needed to understand the mechanisms by which some environmental factors influence pest and disease suppression. Especial attention should be devoted to understanding the dynamics of ecological interactions taking place in the soil and root
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environments that are necessary to achieve successful and reproducible biological control under field conditions (Rosenheim, 1998). Future modeling efforts that view food webs as open and flexible structures that can accommodate changes in species and the dynamics of single and multiple attributes, as recently proposed by De Ruiter et al. (2005), would be extremely useful to improve understanding of the ecosystem service of biological control of pests under scenarios of increased environmental change and disturbance. The partial or complete impairment of the ecosystem service of soil structure maintenance, and thus soil erosion control, is also evident to farmers and land managers through the visual impact of degraded barren lands. Soil erosion losses can be greater than 100 T/ha per year in some hillside agricultural areas (Penning de Vries et al., 1998). Increased stability of soil aggregates upon wetting is perceived as a benefit to soil conservation because it reflects reductions in the rates of soil erosion from intense rainfall events. When soil aggregates break upon wetting into smaller pieces, soil erosion rates are much greater. This observation highlights the importance of biologically-mediated water-stable aggregation for lower soil erosion rates in the field. Furthermore, the ecosystem services of soil erosion control and C sequestration are closely interrelated because they are both influenced by soil aggregate dynamics' impact on soil structure that is largely driven by soil organisms (Six et al., 2002). For example, the accumulation of C in soil under no-till (NT) systems results from a reduction in the rate of aggregate turnover (i.e. aggregate formation vs. disruption) that fosters the formation of stable microaggregates in which C is stabilized and sequestered in the long-term (Six et al., 2000; Six et al., 2002). Further research efforts need to explore methodologies to assess the relative contribution of different soil biota to soil aggregation (i.e. NIRS, AMF-specific glomalin) as affected by climate, soil type, land use, plant species identity, and residue quality.
4.4.
Biological indicators of soil quality and Policy
Increased attention about the potential consequences of biodiversity loss results from the consideration that, if biodiversity affects ecosystem functioning, it is likely to have considerable impacts on the provision of ecosystem goods and services critical for human societies (Swift et al., 2004; Bulte et al., 2005; Jackson et al., 2005; MA, 2005). The important impacts generated by agriculture and other human activities on the soil resource has challenged society with urgent need to find natural resource management strategies that conserve and enhance soil quality and thus are consistent with natural processes that sustain life on earth. Identification of appropriate indicators of soil quality has remained an elusive exercise because it has been complicated by the need to simultaneously address the multiple dimensions of soil function (i.e. ecosystem services), the many physical, chemical and biological factors controlling biogeochemical processes as well as their variability in space and over time (Doran and Safley, 1997). Farmers and land managers need early warning signals and monitoring tools to help them assess the status of their soil; this is because by the time degradation is visible and land productivity reduction evident, it is either too late or too costly to reverse it. Furthermore, the costs of preventing
reductions in land productivity are often much lower than costs of remedial actions (Barrios et al., 2006). Improved capacities to predict and adapt to environmental changes are urgently needed to support local, national, and global policy and decision-making. Most approaches to land quality assessment reported in the literature have looked at the physical and/or chemical characteristics of the soil (Oldeman and van Lynden, 1998). More recent approaches, however, have included integrative measures like NIRS (Shepherd and Walsh, 2002; Velasquez et al., 2005) and biological measures to assess soil quality that benefit from local knowledge of farmers or land managers (Barrios and Trejo, 2003). Biological indicators have the potential to provide early warning because they can capture subtle changes in land quality as a result of their integrative nature that simultaneously reflect changes in physical, chemical and biological characteristics of the soil. Issues of scale are of particular importance when identifying biological indicators of soil quality that can represent the farm, the watershed, the regional and national levels (MA, 2003; Swift et al., 2004; MA, 2005; Bulte et al., 2005). This is essentially because the products of interaction at the system level are often not scale neutral and thus it is necessary to know what level of the hierarchy is being considered when evaluating agroecosystem function (Swift and Anderson, 1993). The development of a minimum set of biological indicators of soil quality continues to be a challenge because of the need to standardize methods to enable comparisons, and the need for a robust sampling strategy in view of spatial and temporal heterogeneity (Swift et al., 2004). One of the most challenging consequences of the limited knowledge of soil biodiversity and function is the difficult process of developing biological monitoring systems that permit an adequate description, measurement and interpretation of the biological properties of soils. Priority research efforts should focus on developing local land quality monitoring systems that inform land users about their land's ecosystem service provision performance. Local monitoring empowerment in rural communities as proposed by Barrios et al. (2006) combined with new economic valuation approaches (Swinton et al., 2006) would support payment for ecosystem services schemes that reward good management practices by land users and thus becomes a further incentive mechanism to sustainable land management.
4.5. Common methodological approaches and training in soil ecology and biodiversity A greater recognition of the contribution of soil biota to the provision of ecosystems services will largely result from increased international collaboration and consensus on methodological approaches at a global scale with an emphasis on biodiversity ‘hot spots’. Effective strategies will include developing common standard methodologies for soil biodiversity inventory, informatics to enhance the soil biodiversity database, assessment of soil processes involved in ecosystem service provision by soil biota, predictive models to quantify the relationship of soil biodiversity to critical ecosystem processes on various spatial scales, field demonstration to farmers, and economic evaluation of ecosystem service provision by soil biota across carefully selected international benchmark site (Swift, 1997; Giller et al., 2005). Each benchmark site might use the
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process of intensification of agricultural practices as an axis for considering the change in significance of biodiversity in regulating ecosystem function (Giller et al., 1997). There is also the need to train national scientists in soil biota natural history, diversity and ecology using experiments that incorporate available information on land use, soil biota and ecosystem processes to develop sustainable soil management options. Given the great diversity of soil biota it remains a great challenge to develop a critical mass of scientists for a thorough study of soil biodiversity and function. As highlighted by Wall and Virginia (2000), different international efforts are needed to facilitate the synthesis of the regional and global distributional patterns of soil biodiversity to fully understand the effects of global change on endemic and introduced species, and to predict how to promote land uses that endure sustainable management of the soil resource.
5.
Conclusions
The sustainable function of natural and agricultural ecosystems is dependent on the contribution of soil organisms to a wide range of ecosystem services. These services have been conceptually organized as those associated with the provision of goods, the regulation of ecosystem processes, and those essential to life on earth. There is continuing need to further identify, study and manage additional groups of soil biota as new methodological approaches and tools become available. The interest in finding ecosystem management entry-points is consistent with conceptual and experimental approaches that concentrate where a large proportion of the biological activity is occurring. Knowledge of hierarchical relationships is also useful to guide potential ecosystem management actions directed to conserve or improve the provision of ecosystem services. A key limitation to the full recognition of soil microorganism contributions to soil processes and ecosystem services has been the difficulty of showing these linkages under field conditions. The adoption of agricultural systems that rest on the biological management of soil processes driven by soil biota may depend on identifying creative ways by which farmers can “see” the impacts made by unseen underground organisms. Greater understanding of aboveground and belowground biodiversity interactions may help ‘raise the profile’ of soil biota because plant biodiversity, being more conspicuous, could provide valuable information about the biodiversity belowground and facilitate soil biota studies beyond the plot scale. It is likely no coincidence that farmers around the world use local plants as indicators of soil quality. The inventory of soil biodiversity and function across agricultural intensification gradients constitutes a useful approach to address the reality of landscapes with multiple land uses and the impact of agriculture on the soil resource. Land conversion and agricultural intensification for increased food production is often a natural response by governments to the increasing population pressure, but often this leads to biodiversity loss. Agricultural sustainability, however, is put at considerable risk because loss of soil biodiversity leads to a reduced capacity for agroecosystem self-regulation and thus increased dependence on external inputs that can only bypass a limited number of biological processes. A lower selfregulation capacity is also closely related with lower resilience
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or capacity of agroecosystems to recover from stress and disturbance brought by environmental change. Knowledge of soil biodiversity and its specific contribution to ecosystem function and the provision of ecosystems services is today limited. Multidimensional approaches that integrate new and existing knowledge are needed for a better understanding of the linkages of soil biodiversity and function to the provision of ecosystem services. Increased efforts to acquire greater knowledge on the spatial and temporal dynamics of functional communities as affected by environmental factors, especially ecosystem service providers, would be critical to increase our predictive understanding of ecosystem service provision. Management of soil biodiversity through the manipulation of plant type and/or soil amendments as well as developing further insights about the effect of scale for designing novel land use systems are major future challenges in agriculture. The economic implications of such diversity to crop productivity and other ecosystem services should be critically evaluated at different spatial and temporal scales. We need to better identify land use and soil management options that lead to favorable trade-offs between agricultural productivity and the provision of ecosystem services.
Acknowledgements This paper is an output of the Global Project “Conservation and Sustainable Management of Below-Ground Biodiversity (CSM-BGBD)” that is coordinated by the Tropical Soil Biology and Fertility Institute of CIAT (TSBF-CIAT) with co-financing from the Global Environment Facility (GEF), and implementation support from United Nations Environment Program (UNEP). Helpful comments provided by Michael J. Swift, Diana Wall, Ken Giller, and two anonymous reviewers and the editor improved the paper and are highly appreciated.
REFERENCES Allen, M.F., Allen, E.B., Gómez-Pompa, A., 2005. Effects of mycorrhizae and non-target organisms on restoration of a seasonal tropical forest in Quintana Roo, Mexico: Factors limiting establishment. Restoration Ecology 13 (2), 325–333. Altieri, M.A., Nichols, C.I., 2003. Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil Tillage Research 72, 203–211. Andersen, J.B., Koch, B., Nielsen, T.H., Sorensen, D., Hansen, M., Nybroe, O., Christopherson, C., Sorenson, J., Molin, S., Givskov, M., 2003. Surface mobility in Pseudomonas sp DSS73 is required for efficient biological containment of the rootpathogenic microfungi Rhizoctonia solani and Phytium ultimum. Microbiology 149, 37–46. Andren, O., Bengtson, J., Clarholm, M., 1995. Biodiversity and species redundancy among litter decomposers. In: Collins, H.P., Robertson, G.P., Klug, M.J. (Eds.), The Significance and Regulation of Soil Biodiversity. Kluwer Academic Publisher, pp. 141–151. Angers, D.A., Recous, S., Aita, C., 1997. Fate of carbon and nitrogen in water-stable aggregates during decomposition of 13C and 15 N-labelled wheat straw in situ. European Journal of Soil Science 48 (2), 295–300.
282
EC O LO GIC A L E CO N O M ICS 6 4 ( 2 00 7 ) 2 6 9 –2 85
Azcon-Aguilar, C., Barea, J.M., 1996. Arbuscular mycorrhizas and biological control of soil-borne pathogens: an overview of the mechanisms involved. Mycorrhiza 4 (6), 457–464. Bagyaraj, D.J., Manjunath, A., Reddy, D.D.R., 1979. Interaction of vesicular arbuscular micorrhiza with root knot nematodes in tomato. Plant and Soil 51, 397–403. Baldani, J.I., Caruso, L., Baldani, V.L.D., Goi, S.R., Dobereiner, J., 1997. Recent advances in BNF with non-legume plants. Soil Biology and Biochemistry 29 (5–6), 911–922. Barea, J.M., Azcon-Aguilar, C., Azcon, R., 1997. Interactions between mycorrhizal fungi and rhizosphere microorganisms within the context of sustainable plant-soil systems. In: Gange, A.C., Brown, V.K. (Eds.), Multitrophic Interactions in Terrestrial Systems. Blackwell Science, Cambridge, pp. 65–77. Barker, K.R., 2003. Perspectives on plant and soil nematology. Annual Review of Phytopathology 41, 1–25. Barrios, E., Trejo, M.T., 2003. Implications of local soil knowledge for integrated soil fertility management in Latin America. Geoderma 111/3–4, 217–231. Barrios, E., Buresh, R.J., Sprent, J.I., 1996a. Organic matter in soil particle size and density fractions from maize and legume cropping systems. Soil Biology and Biochemistry 28 (2), 185–193. Barrios, E., Buresh, R.J., Sprent, J.I., 1996b. Nitrogen mineralization in density fractions of soil organic matter from maize and legume cropping systems. Soil Biology and Biochemistry 28 (10/11), 1459–1465. Barrios, E., Kwesiga, F., Buresh, R.J., Sprent, J.I., 1997. Light fraction soil organic matter and available nitrogen following trees and maize. Soil Science Society of America Journal 61 (3), 826–831. Barrios, E., Kwesiga, F., Buresh, R.J., Sprent, J.I., Coe, R., 1998. Relating preseason soil nitrogen to maize yield in tree legumemaize rotations. Soil Science Society of America Journal 62 (6), 1604–1609. Barrios, E., Delve, R.J., Bekunda, M., Mowo, J., Agunda, J., Ramisch, J., Trejo, M.T., Thomas, R.J., 2006. Soil quality indicators: a South–South development of a methodological guide to integrate local and scientific knowledge. Geoderma 135, 248–259. Barros, E., Curmi, P., Hallaire, V., Chauvel, A., Lavelle, P., 2001. The role of macrofauna in the transformation and reversibility of soil structure of an oxisol in the process of forest to pasture conversion. Geoderma 100 (1/2), 193–213. Beare, M.H., Parmelee, R.W., Hendrix, P.F., Cheng, W., Coleman, D.C., Crossley, D.A., 1992. Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecological Monographs 62 (4), 569–591. Beare, M.H., Pohlad, B.R., Wright, D.H., Coleman, D.C., 1993. Residue placement and fungicide effects on fungal communities in conventional and no-tillage ultisols. Soil Science Society of America Journal 57 (2), 392–399. Beare, M.H., Coleman Jr., D.C., Crossley, D.A., Hendrix, P.F., Odum, E.P., 1995. A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant and Soil 170 (1), 5–22. Blackwood, C.B., Paul, E., 2003. Eubacterial community structure and population size within the soil light fraction, rhizosphere, and heavy fraction of several agricultural systems. Soil Biology and Biochemistry 35 (9), 1245–1255. Blanchart, E., Albrecht, A., Alegre, J., Duboisset, A., Gilot, C., Pashanasi, B., Lavelle, P., Brussaard, L., 1999. Effects of earthworms on soil structure and physical properties. In: Lavelle, P., Brussaard, L., Hendrix, P. (Eds.), Earthworm Management in Tropical Agroecosystems. CAB International, Wallingford, pp. 149–172. Bloem, J., Schouten, T., Didden, W., Akkerhuis, G.J., Keidel, H., Rutgers, M., Breure, T., 2003. Measuring soil biodiversity: experiences, impediments and research needs. Proceedings of
the OECD Expert Meeting on Soil Erosion and Soil Biodiversity Indicators. OECD, Paris, pp. 109–120. Boddey, R.M., Urquiaga, S., Alves, B.J.R., Reis, V., 2003. Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant and Soil 252 (1), 139–149. Bridge, P.D., Prior, C., Sagbohan, J., Lomer, C.J., Carey, M., Buddie, A., 1997. Molecular characterization of isolates of Metarhizium from locust and grasshoppers. Biodiversity and Conservation 6, 177–189. Brown, S., Anderson, J.M., Woomer, P.L., Swift, M.J., Barrios, E., 1994. Soil biological processes in tropical agroecosystems. In: Woomer, P.L., Swift, M.J. (Eds.), The Biological Management of Tropical Soil Fertility. John Wiley and Sons, Chichester, pp. 15–46. Brussaard, L., Behan-Pelletier, V.M., Bignell, D.E., Brown, V.K., Didden, W., Folgarait, P., Fragoso, C., Freckman, D.W., Gupta, V.V.S.R., Hattori, T., Hawksworth, D.L., Klopatek, C., Lavelle, P., Malloch, D.W., Rusek, J., Soderstrom, B., Tiedje, J.M., Virginia, R.A., 1997. Biodiversity and ecosystem functioning in soil. Ambio 26 (8), 563–570. Brussaard, L., Kuyper, T.W., Didden, W.A.M., de Goede, R.G.M., Bloem, J., 2004. Biological soil quality from biomass to biodiversity — importance and resilience to management stress and disturbance. In: Schønning, P., Emholt, S., Christensen, B.T. (Eds.), Managing Soil Quality: Challenges in Modern Agriculture. CAB International, Wallingford, pp. 139–161. Bulte, E., Hector, A., Larigauderie, A., 2005. ecoSERVICES: assessing the impacts of biodiversity changes on ecosystem functioning and services. DIVERSITAS Report No.3. Cambardella, C.A., Elliot, T.E., 1994. Carbon and nitrogen dynamics of soil organic matter fractions from cultivated grassland soils. Soil Science Society of America Journal 58, 123–130. Castillo, P., Nico, A.I., Azcón-Aguilar, C., Del Río Rincón, C., Calvet, C., Jiménez-Díaz, R.M., 2006. Protection of olive planting stocks against parasitism of root-knot nematodes by arbuscular mycorrhizal fungi. Plant Pathology 55, 705–713. Chauvel, A., Grimaldi, M., Barros, E., Blanchart, E., Sarrazin, M., Lavelle, P., 1999. Pasture degradation by an Amazonian earthworm. Nature 389 (6722), 32–33. Cole, J.R., Chai, B., Farris, R.J., Wang, O., Kulam, S.A., McGarrell, D.M., Garrity, G.M., Tiedje, J.M., 2005. The Ribosomal Database Project (RDP II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Research 33, 294–296 Database Issue. Coleman, D.C., Crossley, D.A., Hendrix, P.F., 2004. Fundamentals of Soil Ecology, 2nd Ed. Elsevier Academic Press, Amsterdam–Boston. Costanza, R., d'Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O'Neill, R.V., Paruello, J., Raskin, P.G., Sutton, P., van den Belt, M., 1997. The value of the world's ecosystem services and natural capital. Nature 387, 253–260. Dalal, R.C., Wang, W., Robertson, G.P., Parton, W.J., 2003. Nitrous oxide emission from Australian agricultural lands and mitigation options: a review. Australian Journal of Soil Research 41, 165–195. Decaens, T., Jiménez, J.J., Gioia, C., Measey, G.J., Lavelle, P., 2006. The value of soil animals for conservation biology. European Journal of Soil Biology 42 (1), S23–S38. De Ruiter, P.C., Neutel, A.M., Moore, J.C., 1995. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269, 1257–1260. De Ruiter, P.C., Wolters, V., Moore, J.C., Winemiller, K.O., 2005. Food web ecology: playing Jenga and beyond. Science 309, 68–70. Diaz, S., Cabido, M., 2001. Vive la différence: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16 (11), 646–655. Dong, L.Q., Zhang, K.Q., 2006. Microbial control of plant-parasitic nematodes: a five-party interaction. Plant and Soil 288, 31–45. Doran, J.W., Safley, M., 1997. Defining and assessing soil health and sustainable productivity. In: Pankhurst, C.E., Doube, B.M.,
EC O L O G IC A L E C O N O M IC S 6 4 ( 2 0 07 ) 26 9 –2 85
Gupta, V.V.S.R. (Eds.), Biological Indicators of Soil Health. CAB International, Wallingford, pp. 1–28. Ettema, C.H., Wardle, D.A., 2002. Spatial soil ecology. Trends in Ecology and Evolution 17 (4), 177–183. Food and Agriculture Organization (FAO), 2003. AEZWIN: An interactive multiple-criteria analysis tool for land resources appraisal. FAO Land and Water Digital Media Series, vol. 15. Frey, S.D., Elliot, E.T., Paustian, K., 1999. Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biology and Biochemistry 31 (4), 573–585. George, E., Haussler, K., Kothari, S.K., Li, X.L., Marschner, H., 1992. Contribution of mycorrhizal hyphae to nutrient and water uptake by plants. In: Read, D.J., Lewis, D.H., Fitter, A.H., Alexander, I.J. (Eds.), Mycorrhizas in Ecosystems. CAB International, Wallingford, pp. 42–48. Giller, K.E., 2001. Nitrogen Fixation in Tropical Cropping Systems, 2nd Edn. CAB International, Wallinford. Giller, K.E., Beare, M.H., Lavelle, P., Izac, A.M., Swift, M.J., 1997. Agricultural intensification, soil biodiversity and agroecosystem function. Applied Soil Ecology 6 (1), 3–16. Giller, K.E., Bignell, D., Lavelle, P., Swift, M.J., Barrios, E., Moreira, F., van Noordwijk, M., Barois, I., Karanja, N., Huising, J., 2005. Soil biodiversity in rapidly changing tropical landscapes: scaling down and scaling up. In: Bardgett, R., Usher, M.B., Hopkins, D.W. (Eds.), Biological Diversity and Function in Soils. Cambridge University Press, Cambridge, pp. 295–318. Haas, D., Keel, C., 2003. Regulation of antibiotic production in rootcolonizing Pseudomonas spp. And relevance for biological control of plant disease. Annual Review of Phytopatology 41, 117–153. Haas, D., Défago, G., 2005. Biological control of soil-borne pathogens by fluorescent Pseudomonads. Nature Reviews in Microbiology 3, 307–319. Hedde, M., Lavelle, P., Joffre, R., Jiménez, J.J., Decaens, T., 2005. Specific functional signature in soil macro-invertebrate biostructures. Functional Ecology 19, 785–793. Hooper, D.U., Chapin III, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., Vandermeer, J., Wardle, D.A., 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75 (1), 3–35. Hungria, M., Campo, R.J., Mendez, I.C., 2003. Benefits of inoculation of common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biology and Fertility of Soils 39, 88–93. Hunt, H.W., Coleman, D.C., Ingham, E.R., Ingham, R.E., Elliot, E.T., Moore, J.C., Rose, S.L., Rid, C.F.F., Morley, C.R., 1987. The detrital food web in a shortgrass prairie. Biology and Fertility of Soils 3 (1/2), 57–68. Hunt, H.W., Wall, D.H., 2002. Modeling the effects of loss of soil biodiversity on ecosystem function. Global Change Biology 8 (1), 33–50. Hurst, M.R., Glare, T.R., Jackson, T.A., 2004. Cloning Serratia entomophila antifeeding genes — a putative defective prophage active against the grass grub Costelytra zealandica. Journal of Bacteriology 186 (15), 5116–5128. Jackson, L, Bawa, K., Pascual, U., Perrings, C., 2005. agroBIODIVERSITY: A new science agenda for biodiversity in support of sustainable agroecosystems. DIVERSITAS Report#4. Jackson, T.A., 2003. Using entomopathogens in scarab pest management. In: Aragón, G., Morón, M.A., Marín, A. (Eds.), Estudios sobre coleópteros del suelo en América. Publicación especial de la Benemérita Universidad Autónoma de Puebla, México, pp. 327–335. Jackson, T.A., Pearson, J.F., O'Callaghan, M.;, Mahanty, H.K., Willocks, M., 1992. Pathogen to product - development of Serratia entomophila (Enterobacteriaceae) as a commercial biological
283
control agent for the New Zealand grass grub (Costelytra zealandica). In: Jackson, T.A., Glare, T.R. (Eds.), Use of Pathogens in Scarab Pest Management. Intercept, Andover, U.K., pp. 191–198. Jaizme-Vega, M.C., Tenoury, P., Pinochet, J., Jaumont, M., 1997. Interactions between the root-knot nematode Meloidogyne incognita and Glomus mosseae in banana. Plant and Soil 196 (1), 27–35. Jakobsen, I., Abbott, L.K., Robson, A.D., 1992. External hyphae of vesicular arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 120 (3), 371–380. Johnson, N.C., Graham, J.H., Smith, F.A., 1997. Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytologist 135 (4), 575–586. Kandeler, E., Palli, S., Stemmer, M., Gerzabek, M.H., 1999. Tillage changes microbial biomass and enzyme activities in particlesize fractions of a Haplic Chernozem. Soil Biology and Biochemistry 31 (9), 1253–1264. Kasiamdari, R.S., Smith, S.E., Smith, F.A., Scott, E.S., 2002. Influence of the mycorrhizal fungus, Glomus Coronatum, and soil phosphorus on infection and disease caused by binucleate Rhizoctonia and Rhizoctonia solani on mung bean (Vigna radiata). Plant and Soil 238 (2), 235–244. Keller, S., Schweizer, C., Keller, E., Brenner, H., 1997. Control of white grubs (Melolontha melolontha L.) by treating adults with the fungus Beauveria brongniartii. Biocontrol Science and Technology 7, 105–116. Ladha, J.K., Reddy, P.M., 2003. Nitrogen fixation in rice systems: State of knowledge and future prospects. Plant and Soil 252 (1), 151–167. Lavelle, P., Spain, A.V., 2001. Soil Ecology. Kluwer Academic Publishers, The Netherlands. Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P., Ineson, P., Dhillion, O.W., 1997. Soil function in a changing world: The role of invertebrate ecosystem engineers. European Journal of Soil Biology 33 (4), 159–193. Laville, J., Voisard, C., Keel, C., Maurhofer, M., Défago, G., Haas, D., 1992. Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proceedings of the National Academy of Sciences 89, 1562–1566. Ledgard, S.F., 1991. Transfer of fixed nitrogen from white clover to associated grasses in swards grazed by dairy cows estimated using 15N methods. Plant and Soil 131 (2), 215–223. Lendzemo, V.W., Kuyper, T.W., Kropff, M.J., van Ast, A., 2005. Field inoculation with arbuscular mycorrhizal fungi reduces Striga hermonthica performance on cereal crops and has the potential to contribute to integrated Striga management. Field Crops Research 91 (1), 51–61. Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A., Hooper, D.U., Huston, M.A., Raffaelli, D., Schmid, B., Tilman, D., Wardle, D.A., 2001. Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294, 804–808. Lynch, J.M., Benedetti, A., Insam, H., Nuti, M.P., Smalla, K., Torsvik, V., Nannipieri, P., 2004. Microbial diversity in soil: ecological theories, the contribution of molecular techniques and the impact of transgenic plants and transgenic microorganisms. Biology and Fertility of Soils 40 (6), 363–385. Mallarino, A.P., Wedin, W.F., Goyenola, R.S., Perdomo, C.H., West, C.P., 1990a. Legume species and proportion effects on symbiotic dinitrogen fixation in legume–grass mixtures. Agronomy Journal 82, 785–789. Mallarino, A.P., Wedin, W.F., Perdomo, C.H., Goyenola, R.S., West, C.P., 1990b. Nitrogen transfer from white clover, red clover, and birdsfoot trefoil to associated grass. Agronomy Journal 82 (4), 790–795. Mando, A., Stroosnijder, L., Brussaard, L., 1996. Effects of termites on infiltration into crusted soil. Geoderma 74 (1/2), 107–113.
284
EC O LO GIC A L E CO N O M ICS 6 4 ( 2 00 7 ) 2 6 9 –2 85
Mando, A., Miedema, R., 1997. Termite-induced change in soil structure after mulching degraded (crusted) soil in the Sahel. Applied Soil Ecology 6 (3), 241–249. Marshner, H., 1995. Mineral Nutrition of Higher Plants, 2nd Ed. Academic Press, London. Millennium Ecosystem Assessment (MA), 2003. Ecosystem and Human Well-Being: A Framework for Assessment. Island Press, Washington, DC. Millennium Ecosystem Assessment (MA), 2005. Ecosystem and Human Well-Being: Synthesis. Island Press, Washington, DC. Miller, R.M., Jastrow, J.D., 2000. Mycorrhizal fungi influence soil structure. In: Kapulnik, Y., Douds, D.D. (Eds.), Arbuscular Mycorrhizas: Molecular Biology and Physiology. Kluwer Academic Press, Dordrecht, pp. 3–18. Miller, R.M., Kling, M., 2000. The importance of integration and scale in the arbuscular mycorrhizal symbiosis. Plant and Soil 226 (2), 295–309. Moore, J.C., De Ruiter, P.C., 2000. Invertebrates in detrital food webs along gradients of productivity. In Invertebrates as Webmasters in Ecosystems. In: Coleman, D.C., Hendrix, P.F. (Eds.), CABI Publishing, Wallingford, U.K., pp. 161–184. Mummey, D.L., Rillig, M.C., Six, J., 2006. Endogeic earthworms differentially influence bacterial communities associated with different soil aggregate size fractions. Soil Biology and Biochemistry 38 (7), 1608–1614. Oades, J.M., 1984. Soil organic matter and structural stability: mechanisms and implications for management. Plant and Soil 76 (1/3), 319–337. Oldeman, L.R., van Lynden, G.W.J., 1998. Revisiting the GLASOD methodology. In: Lal, R., Blum, W.H., Valentine, C., Stewart, B.A. (Eds.), Methods for Assessment of Soil Degradation. CRC Press, New York, pp. 423–440. Penning de Vries, F.W.T., Agus, F., Kerr, J. (Eds.), 1998. Soil Erosion at Multiple Scales: Principles and methods for assessing causes and impacts. CABI publishing. Phiri, S., Barrios, E., Rao, I.M., Singh, B., 2001. Changes in soil organic matter and phosphorus fractions under planted fallows and a crop rotation system on a Colombian volcanicash soil. Plant and Soil 231 (2), 211–223. Potter, D.A., 1998. Destructive Turfgrass Insects: Biology, Diagnosis and Control. Ann Arbor Press, Chelsea, MI. Radajewski, S., Ineson, P., Parekh, N.R., Murrel, J.C., 2000. Stable isotope probing as a tool in microbial ecology. Nature 403, 646–649. Rao, I.M., Barrios, E., Amézquita, E., Friesen, D.K., Thomas, R., Oberson, A., Singh, B.R., 2004. Soil phosphorus dynamics, acquisition and cycling in crop-pasture-fallow systems in low fertility tropical soils: a review from Latin America. In: Delve, R.J., Probert, M.N.E. (Eds.), Modeling nutrient management in tropical cropping systems. ACIAR proceedings, vol. 114, pp. 126–134. Camberra. Requena, N., Pérez-Solis, E., Azcón-Aguilar, C., Jeffries, P., Barea, J.M., 2001. Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Applied and Environmental Microbiology 67 (2), 495–498. Rillig, M., Wright, S.F., Eviner, V.T., 2002. The role of arbuscular mycorrhizal fungi and glomalin on soil aggregation: comparing the effects of five plant species. Plant and Soil 238 (2), 325–333. Rillig, M., 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7 (8), 740–754. Ritz, K., McHugh, M., Harris, J., 2003. Biological diversity and function in soils: contemporary perspectives and implications in relation to the formulation of effective indicators. OECD expert meeting on soil erosion and soil biodiversity indicators. OECD, Rome. Robertson, G.P., Paul, E.A., Hardwood, R.R., 2000. Greenhouse gases in intensive agriculture: Contributions of individual gases to
the radiative forcing of the atmosphere. Science 289, 1922–1925. Rosenheim, J.A., 1998. Higher order predators and the regulation of insect herbivore populations. Annual Review of Entomology 43, 421–447. Sánchez, P.A., Shepherd, K.D., Soule, M.J., Place, F.M., Buresh, R.J., Izac, A.M., Mokwunye, A.U., Kwesiga, F.R., Ndiritu, C.G., Woomer, P.L., 1997. Soil Fertility Replenishment in Africa: An Investment in Natural Resource Capital. In: Buresh, R.J., Sánchez, P.A., Calhoun, F. (Eds.), Replenishing Soil Fertility in Africa. SSSA special publication, vol. 51, pp. 1–46. Madison. Schmidt, O., Curry, J.P., Dyckmans, J., Rota, E., Scrimgeour, C.M., 2004. Dual stable isotope analysis (delta13C and delta15) of soil invertebrates and their food sources. Pedobiologia 48, 171–180. Senapati, B.K., Lavelle, P., Giri, S., Pashanasi, B., Alegre, J., Decaens, T., Jiménez, J.J., Albrecht, A., Blanchart, E., Mahieux, M., Rousseaux, L., Thomas, R., Panigrahi, P.K., Venkatachalan, 1999. M., Soil earthworm technologies for tropical ecosystems. In: Lavelle, P., Brussard, L., Hendrix, P.F. (Eds.), Earthworm Management in Tropical Agroecosystems. CAB International, Wallingford, pp. 199–238. Sessitsch, A., Weilharter, A., Gerzabek, M.H., Kirchmann, H., Kandeler, E., 2001. Microbial population structures in soil particle size fractions of a long term fertilizer field experiment. Applied and Environmental Microbiology 67 (9), 4215–4224. Shepherd, K.D., Walsh, M.G., 2002. Development of reflectance spectral libraries for characterization of soil properties. Soil Science Society of America Journal 66, 988–998. Six, J., Elliot, E.T., Paustian, K., Doran, J.W., 1998. Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Science Society of America Journal 62, 1367–1377. Six, J., Elliot, E.T., Paustian, K., 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology and Biochemistry 32, 2099–2103. Six, J., Feller, C., Denef, K., Ogle, S.M., Moraes Sa, J.C., Albrecht, A., 2002. Soil organic matter, biota and aggregation in temperate and tropical soils — Effects of no-tillage. Agronomie 22 (7/8), 755–775. Smith, S.E., Read, D.J., 1997. Mycorrhizal Symbiosis, 2nd Edn. Academic Press, New York. Susilo, F.X., Neutel, A.M., van Noordwijk, M., Hairiah, K., Brown, G., Swift, M.J., 2004. Soil biodiversity and food webs. In: van Noordwijk, M., Cadisch, G., Ong, C.K. (Eds.), Below-ground Interactions in Tropical Agroecosystems. CAB International, Wallingford, pp. 285–302. Swift, M.J., 1997. Soil biodiversity, agricultural intensification and agroecosystem function. Special Issue Applied Soil Ecology 6 (1), 1–108. Swift, M.J., 1998. Towards the second paradigm: integrated biological management of soil. In: Siqueira, J.O., Moreira, J.O., Lopes, F.M.S., Guilherme, A.S., Faquin, L.R.G., Furtani Neto, V., Carvalho, A.E. (Eds.), Inter-relação Fertilidade, Biologia do Solo e Nutrição de Plantas. UFLA, Lavras, pp. 11–24. Swift, M.J., Anderson, J.M., 1993. Biodiversity and ecosystem function in agricultural systems. In: Schulze, E.D., Mooney, H.A. (Eds.), Biodiversity and ecosystem function. Ecological Studies, vol. 99. Springer-Verlag, Berlin, pp. 14–41. Swift, M.J., Heal, O.W., Anderson, J.M., 1979. Decomposition in terrestrial ecosystems. University of California Press, Berkeley. Swift, M.J., Izac, A.M.N., van Noordwijk, M., 2004. Biodiversity and ecosystem services in agricultural landscapes — are we asking the right questions? Agriculture, Ecosystems & Environment 104, 113–134. Swinton, S.M., Lupi, F., Robertson, G.P., Landis, D.A., 2006. Ecosystem services from agriculture: looking beyond the usual suspects. American Journal of Agricultural Economics 88 (5), 1160–1166.
EC O L O G IC A L E C O N O M IC S 6 4 ( 2 0 07 ) 26 9 –2 85
Tiedje, J.M., Cho, J.C., Murray, A., Teves, D., Xia, B., Zhou, J., 2001. Soil teeming with life: new frontiers to soil science. In: Rees, R.M., Ball, B.C., Campbell, C.D., Watson, C.A. (Eds.), Sustainable Management of Soil Organic Matter. CAB International, Wallingford, pp. 393–412. Tisdal, J.M., Oades, J.M., 1982. Organic matter and water stable aggregates in soils. Journal of Soil Science 33, 141–163. Torsvik, V., Goksoyr, J., Daae, F.L., Sorheim, R., Michalsen, J., Salte, K., 1994. Use of DNA analysis to determine the diversity of microbial communities. In: Ritz, K., Dighton, J., Giller, K.E. (Eds.), Beyond the Biomass. John Wiley, Chichester, pp. 39–48. UNCED (United Nations Congress on Environment and Development), 1992. Agenda 21. United Nations, Geneva. UNEP (United Nations Environment Program), 1995. Global Biodiversity Assessment. University Press, Cambridge. Van der Putten, W.H., De Ruiter, P.C., Bezemer, T.M., Harvey, J.A., Wassen, M., Wolters, V., 2004. Trophic interactions in a changing world. Basic and Applied Ecology 5, 487–494. Velasquez, E., Lavelle, P., Barrios, E., Joffre, R., Reversat, F., 2005. Evaluating soil quality in tropical agroecosystems of Colombia using NIRS. Soil Biology and Biochemistry 37 (5), 889–898. Wall, D.H., Moore, J.C., 1999. Interactions underground: soil biodiversity, mutualism and ecosystem processes. BioScience 49 (2), 109–117. Wall, D.H., Virginia, R.A., 2000. The world beneath our feet: Soil Biodiversity and Ecosystem Functioning. In: Raven, P.H., Williams, T. (Eds.), Nature and Human Society: The quest for a
285
Sustainable World. Committee for the Second Forum on Biodiversity, National Academy of Sciences and National Research Council, Washington D.C., pp.225–241. Wall, D.H., Adams, G., Parsons, A.N., 2001. Soil Biodiversity. In: Chapin III, F.S., Sala, O.E., Huber-Sannwald, E. (Eds.), Global biodiversity in a changing environment: Scenarios for the 21st century. Springer-Verlag, New York, pp. 47–82. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., Van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633. Wardle, D.A., Yeates, G.W., Barker, G.M., Bonner, K.I., 2006. The influence of plant litter diversity on decomposer abundance and diversity. Soil Biology and Biochemistry 38, 1052–1062. Woomer, P.L., Swift, M.J., 1994. The Biological Management of Tropical Soil Fertility. John Wiley and Sons, Chichester. Wright, S.F., Upadhyaya, A., 1996. Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Science 161 (9), 575–586. Wright, S.F., Upadhyaya, A., 1998. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil 198 (1), 97–107. Wu, L., Thompson, D.K., Liu, X., Fields, M.W., Bagwell, C.E., Tiedje, J.M., Zhou, J., 2004. Development and evaluation of microarraybased whole-genome hybridization for detection of microorganisms within the context of environmental applications. Environmental Science and Technology 38 (24), 6775–6782.