A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics

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A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics
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  Soil & Tillage Research 79 (2004) 7–31 Review A history of research on the link between (micro)aggregates,soil biota, and soil organic matter dynamics  J. Six a , b , ∗ , H. Bossuyt c , S. Degryze d , K. Denef  b a  Department of Agronomy and Range Science, University of California, Davis, CA 95616, USA b  Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO 80523, USA c  Institute of Ecology, University of Georgia, Athens, GA 30602, USA d  Laboratory for Soil Fertility and Soil Biology, K.U. Leuven, Kasteelpark Arenberg 20, 3001 Heverlee, Belgium Received 19 March 2003; received in revised form 18 December 2003; accepted 19 March 2004 Abstract Since the 1900s, the link between soil biotic activity, soil organic matter (SOM) decomposition and stabilization, andsoil aggregate dynamics has been recognized and intensively been studied. By 1950, many studies had, mostly qualitatively,investigated the influence of the five major factors (i.e. soil fauna, microorganisms, roots, inorganics and physical processes)on this link. After 1950, four theoretical mile-stones related to this subject were realized. The first one was when Emerson[Nature 183 (1959) 538] proposed a model of a soil crumb consisting of domains of oriented clay and quartz particles.Next, Edwards and Bremner [J. Soil Sci. 18 (1967) 64] formulated a theory in which the solid-phase reaction between clayminerals, polyvalent cations and SOM is the main process leading to microaggregate formation. Based on this concept,Tisdall and Oades [J. Soil Sci. 62 (1982) 141] coined the aggregate hierarchy concept describing a spatial scale dependenceof mechanisms involved in micro- and macroaggregate formation. Oades [Plant Soil 76 (1984) 319] suggested a small,but very important, modification to the aggregate hierarchy concept by theorizing the formation of microaggregates withinmacroaggregates. Recent research on aggregate formation and SOM stabilization extensively corroborate this modificationand use it as the base for furthering the understanding of SOM dynamics. The major outcomes of adopting this modificationare: (1) microaggregates, rather than macroaggregates protect SOM in the long term; and (2) macroaggregate turnover isa crucial process influencing the stabilization of SOM. Reviewing the progress made over the last 50 years in this area of research reveals that still very few studies are quantitative and/or consider interactive effects between the five factors. Thequantification of these relationships is clearly needed to improve our ability to predict changes in soil ecosystems due tomanagement and global change. This quantification can greatly benefit from viewing aggregates as dynamic rather than staticentities and relating aggregate measurements with 2D and 3D quantitative spatial information.© 2004 Elsevier B.V. All rights reserved. Keywords:  Aggregate; Dry–wet cycle; Earthworm; Freeze–thaw cycle; History; Root; Soil biota; Soil organic matter  This publication is dedicated to Ted Elliott who personallytaught many of the concepts described here and is in many ways“the grandfather” of many of the ideas expressed here. ∗ Corresponding author. Tel.:  + 1-530-752-1212;fax:  + 1-530-752-4361.  E-mail address:  jwsix@ucdavis.edu (J. Six). 1. Introduction The interest in long-term sustainability and reduc-tion of environmental costs of agricultural ecosys-tems have emerged and only recently augmented. Toachieve this interest, soil organic matter (SOM) dy- 0167-1987/$ – see front matter © 2004 Elsevier B.V. All rights reserved.doi:10.1016/j.still.2004.03.008  8  J. Six et al./Soil & Tillage Research 79 (2004) 7–31 namics and nutrient cycling need to be better under-stood and subsequently managed. In trying to furtherour understanding of these important dynamic soilproperties, recent research focuses often on the roleplayed by the soil matrix, the soil biota and their mul-tiple interactions. It is this multitude of interactionsthat makes it a very complex research subject to beelucidated.Studies tackling this complexity often use aggre-gate measurements as surrogates of the, in itself, com-plex soil matrix. Aggregates not only physically pro-tect soil organic matter (e.g. Tisdall and Oades, 1982),but also influence microbial community structure (e.g.Hattori, 1988), limit oxygen diffusion (e.g. Sexstoneet al., 1985), regulate water flow (e.g. Prove et al.,1990), determine nutrient adsorption and desorption(e.g. Linquist et al., 1997; Wang et al., 2001), andreduce run-off and erosion (e.g. Barthes and Roose,2002). All of these processes have profound effects onSOM dynamics and nutrient cycling.The objective of the first section of this review is togiveahistoricalaccountofthedevelopmentoftheoriesrelated to aggregate–SOM interactions. In the secondsection influences and interactions between the majorfactors controlling aggregation are synthesized with aspecial reference to microaggregation and macroag-gregate turnover. 2. Historical development of theoreticalaggregate–SOM models 2.1. Before 1950 All major factors playing a role in aggregate for-mation and stabilization were already identified in theearly 1900s. By then, it was already clear that thefollowing factors influenced soil aggregation: (1) soilfauna; (2) soil microorganisms; (3) roots; (4) inor-ganic binding agents; and (5) environmental variables(Fig. 1). The most extensively studied group of soilfauna in relation to aggregation is the earthworms. Re-cently, termites have received a well-deserved greaterattention for their significant involvement in soil struc-tural building. Mycorrhizal and saprophytic fungi arethe most important soil microorganisms involved inthe formation and stabilization of aggregates, but alsobacteria can have profound influences on aggregation,especially at the microscale. Penetrating roots can me-chanically break up existing aggregates, but they alsostabilize surrounding aggregates through drying thesoil and root exudation with its associated microbialactivity. Most studies investigating the relationship be-tween inorganic binding agents and aggregation havefocused on calcium and oxyhydroxides. The promi-nent impact of the physical processes of drying andwetting plus freezing and thawing on both the forma-tion and the degradation of aggregation is well known.The impact of these five factors on aggregation andthe interactions and feedbacks between the five factorsare described in some very comprehensive reviewspublished in the 1950s–early 1960s: Martin et al.(1955), Henin et al. (1958), Greenland (1965a,b), Harris et al. (1966), Kemper and Koch (1966). Their excellent syntheses will not be repeated in this review,but a short summary will be provided as a referral.Martin et al. (1955) described in detail the positiveinfluence of organic residues, microbial activity, syn-thetic soil conditioners and exchangeable cations onsoilaggregation.Heninetal.(1958)revieweddifferentmethodologies to measure aggregate stability and usedthem to develop an instability index strongly relatedto soil functioning (i.e. the instability index of a soilis directly related to its infiltration rate). An in depthdescription of the interactions between clays and or-ganic compounds with specific reference to the influ-ence of mineralogy and oxides is given by Greenland(1965a,b). Harris et al. (1966) focused on the biologi- cal (i.e. microbial activity and earthworms) and envi-ronmental factors and how they are affected by agri-cultural practices. They also gave a detailed accountof the chemical reactions involved in the formation of aggregates. One of the very few attempts to quantifythe relationships between these factors and aggregatestability was done by Kemper and Koch (1966).It is evident from these reviews that before 1950,very little effort was made to develop theoreticalframeworks of aggregate formation and the relation-ships between SOM, roots, soil fauna, soil microor-ganisms, physical processes and inorganic bindingagents were little or not at all quantified. 2.2. After 1950 In this section, all studies considered critical forour current understanding of aggregate–SOM dynam-   J. Six et al./Soil & Tillage Research 79 (2004) 7–31  9Fig. 1. The multiplicity of interactions and feedbacks between the five major factors influencing aggregate formation and stabilization. ics are chronologically described (Fig. 2). The firstaggregate–SOM conceptual model, based on the cur-rent theory at that time, was proposed by Emerson(1959). Emerson (1959) described how a soil crumb consisted of domains of oriented clays and quartz par-ticles. According to the Emerson model, SOM in-creased the stability of a soil crumb by linking to-gether domains of oriented clays and quartz parti-cles. The process of slaking was consequently un-derstood as the breaking of quartz-domain bonds bythe crystalline swelling of clay domains upon wetting.Emerson (1977), based on his model, argued that theamount of protected SOM is proportional to the sur-face area of the domains. In other words, only a mono-layer of SOM can be associated with the domain sur-face. This monolayer of SOM is stabilized betweenclay domains by being cross-linked through Al, Fe andhydrogen bonds.Edwards and Bremner (1967) proposed the nextmajor theoretical stepping stone. They presented themicroaggregate theory in which the formation of mi-croaggregateswasenvisionedasasolid-phasereactionbetween organic matter, polyvalent metals and electri-cally neutral clays. They rejected Emerson’s model of aggregates containing sand grains as primary buildingblocks. According to Edwards and Bremner (1967),the only highly stable aggregates are fine sand- andsilt-sized microaggregates ( < 250  m) consisting of clay–polyvalent metal–organic matter complexes. Mi-croaggregatesareformedbybondingofC–P–OMclaysized units, where C: clay particle, P: polyvalent metal(Fe, Al, Ca) and OM: organo-metal complex, and arerepresented as [(C–P–OM) x ] y . It is evident that theC–P–OM units are equivalent to the clay domains of Emerson. However, Edwards and Bremner (1967) en-visioned C–P–C and OM–P–OM units too. They alsopostulated that the organic matter complexed into themicroaggregates would be inaccessible to microorgan-isms and physically protected.The aggregate hierarchy concept proposed byTisdall and Oades (1982) is probably the most signif-icant theoretical advancement in the understanding of aggregate–SOM interactions. In the aggregate hierar-chy concept it is postulated that the different bindingagents (i.e. transient versus temporary versus persis-tent binding agents) act at different hierarchical stagesof aggregation. Free primary particles and silt-sizedaggregates( < 20  m)areboundtogetherintomicroag-gregates (20–250  m) by persistent binding agents(i.e. humified organic matter and polyvalent metalcation complexes), oxides and highly disordered alu-minosilicates. These stable microaggregates, in turn,  10  J. Six et al./Soil & Tillage Research 79 (2004) 7–31 Fig. 2. A time line of the critical advancements in the understanding of soil organic matter–aggregation interactions. are bound together into macroaggregates (>250  m)by temporary (i.e. fungal hyphae and roots) and tran-sient (i.e., microbial- and plant-derived polysaccha-rides) binding agents. However, the polysaccharidesare believed to mostly exert their binding capacity ona scale  < 50  m within the macroaggregates. Becauseof this hierarchical order of aggregates and theirbinding agents, microaggregate stability is higherand less dependent on agricultural management thanmacroaggregate stability.Two years after the publication of the aggregatehierarchy theory, Oades (1984) formulated a small,but later to be found very important, modification tothe concept of the hierarchical build up of aggregates(Fig. 3). In the hierarchical aggregate model of  Tisdall andOades(1982),itwasimplicitlyunderstoodthatag-gregates are sequentially formed, i.e. microaggregatesare first formed free and then serve as the buildingblocks for the formation of macroaggregates. Oades(1984), on the other hand, postulated that the rootsand hyphae holding together the macroaggregate formthe nucleus for microaggregate formation in the cen-ter of the macroaggregate. Since roots and hyphae aretemporary binding agents, they do not persist and de-compose into fragments. These fragments coated withmucilagesproducedduringdecompositionbecomeen- Macroaggregates (> 250 µ m) Microaggregates (20-250 µ m) Primary Particles (< 20 µ m)    T   i  s   d  a   l   l  a  n   d   O  a   d  e  s   (   1   9   8   2   ) O          a       d           e       s           (            1          9           8           4               )           Fig. 3. The opposing chronology of the formation of the hierar-chical aggregate orders implicitly described by Tisdall and Oades(1982) vs. postulated by Oades (1984).   J. Six et al./Soil & Tillage Research 79 (2004) 7–31  11 crusted with clays resulting in the inception of a mi-croaggregate within a macroaggregate.Elliott (1986) tested the aggregate hierarchy modelfor North American grassland soils and applied it toexplain the loss of SOM upon cultivation. As a di-rect consequence of the concept of microaggregatesbeing bound together by SOM into macroaggregates,Elliott (1986) hypothesized that macroaggregates con-tain more labile and less highly processed SOM thanmicroaggregates and that this SOM is lost upon culti-vation. His hypothesis was corroborated and it identi-fied for the first time the direct link between agricul-tural disturbance, decreased aggregation and loss of labile SOM. Based on these concepts, two sets of ob-servations can be used to identify the existence of anaggregate hierarchy in a soil: (1) an increase in C con-centration with increasing aggregate-sized class; and(2) a higher content of new and more labile (e.g. hav-ing a higher C:N ratio) C in macroaggregates than inmicroaggregates.Elliott and Coleman (1988) adopted the conceptof microaggregate formation within macroaggregatesfrom Oades (1984) and ascribed this microaggregateformation to the anaerobic and resulting reducing con-ditions in the center of the macroaggregates. Theyalso described, as a mirror image of the aggregate hi-erarchy, four hierarchical pore categories: (1) macro-pores; (2) pore space between macroaggregates; (3)pores between microaggregates but within macroag-gregates; and (4) pores within microaggregates. Thishierarchical pore structure facilitates the understand-ing of how pore networks determine the links betweenorganisms in a soil food web. The macropores housemicroarthropods; nematodes move through the poresbetween macroaggregates; protozoa, small nematodesand fungi inhabit the pore space between microaggre-gates; bacteria are protected within the pores of themicroaggregates.Based on the hierarchical order of soil aggregationby Hadas (1987), which is very similar to the one of Tisdall and Oades (1982), Dexter (1988) formulated the “porosity exclusion principle”. The porosity ex-clusion principle states that the aggregates of a lowerhierarchical order exclude the pore spaces betweenthe building blocks of the aggregates of a higher hier-archical order. Because pores form cavities and fail-ure planes, the excluded porosity in aggregates of alower order causes their greater density and internalstrength compared to aggregates in a higher order.This “porosity exclusion principle” is similar to thatgiven by Currie (1966). Kay (1990) took the “poros- ity exclusion principle” a step further by arguing thatthe effectiveness of different binding agents would de-pend on their dimensions relative to the size of thepores or failure planes that need to be bridged to bindparticles together. Hence, inorganic and organic sta-bilizing compounds with their small dimensions areabletostabilizemicroaggregates,butrootsandhyphaewill have to act as binding agents between particlesseparated by greater distances or pores. It is evidentthat the pore exclusion principle and the hierarchi-cal aggregate model both lead to the same hierarchi-cal relationship between binding agents and aggregateorders.Shipitalo and Protz (1989) presented a model formicroaggregate formation within worm casts. Thismodel contrasts with others models of aggregateformation because it describes how earthworms di-rectly promote the formation of organic matter-coredmicroaggregates. Soil and litter ingestion and subse-quent peristalsis by earthworms fragments litter andcompletely destroys the pre-existing microstructure of a soil. During gut transit, however, clay minerals andorganic materials are intimately mixed and becomeencrusted with mucus to create a new nucleus formicroaggregate formation. Within the excreted casts,drying and aging (i.e. thyxotropic hardening) facili-tate the strengthening of the bonds between organicmaterials, mucus and minerals to stabilize the newlyformed microaggregates.In addition to the two tests for aggregate hierarchybased on the concepts of  Elliott (1986) (see above), anelegant third test was developed by Oades and Waters(1991). They argued that if a soil expresses an aggre-gate hierarchy, macroaggregates will gradually break down into microaggregates before they dissociate intoprimary particles, as an increasing dispersive energyis applied to the soil. They utilized this line of thoughtby measuring the water-stable aggregate distributionof a soil after exposing it to a gradient of increasingdispersive energy: (1) slow wetting; (2) fast wetting;(3) 16h shaking; and (4) sonication. The methodol-ogy was employed to two Alfisols, a Mollisol and anOxisol and resulted in the confirmation of an aggre-gate hierarchy for the two Alfisols and the Mollisol,but not for the Oxisol. Oades and Waters (1991) con-
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