0038-075C/00/1651-73--86 January 2000 Science Vol. 165, No. 1 Copyright Q 2000 by Lippincott Williams &Wilkins, Inc. Printed in U.S.A.

ECOLOGICAL CHALLENGES FOR

I Soil Science integrates specific contributions from physics, chemistry, biology, and the human sciences. During the last 2 decades, these ap- proaches, which had primarily developed separately and at different speeds, have been progressively integrated. has contributed a significant number of integrative concepts and questions, some, such as nutrient cycling and energy budgets, that are rather old, and others, such as soil engineering by macroinvertebrates, the relationship between bio- diversity and soil function, and the impact of landscape fractionation, that are more recent. An important issue common to all disciplines in Soil Science is that of scales. Ecological studies have shown that similar activities, e.g., the building of solid structures by invertebrates for their sheltering or gut transit of soil for digestion, may affect soil function at different scales, affecting the rates of processes in sometimes opposite directions. The concept of functional domains in soil, derived from soil ecological re- search, defines a scale at which physical, chemical, and biological processes can be studied efficiently in a true multidisciplinary approach. Functional domains are specific sites in defined by a main organic resource (leaflitter or ), a major regulator, biotic (i.e., an invertebrate 'engineer' or roots) or abiotic (like freezing/ thawing or drying/rewetting alternates), a set of structures created by the regulator (for example, fecal pellets, galleries, or cracks), and a community of de- pendent invertebrates of smaller size and that live in these structures. Functional domains may be physically identified in soils and specifically studied using the different disciplinary approaches. Spe- cific micromorphologic, isotopic, and other techniques allow us to ad- dress issues at this scale adequately. Ecological research also provides a theoretical background for management of soils at the larger integrative scales of landscape and regions. Essential issues for the near future should use this interdisciplinary ap- proach. Sustainability of cropping systems and maintenance of soil services depend more on an integrated approach than do the extreme developments in single disciplines in isolation that originated the series of problems we now face: large scale , nutrient transfers to neighboring , threats of genetically modified or- ganisms, or accidents. (Soil Science 2000;165:73-86)

Key words: Functional domains, invertebrates, sùstainability, scales, hierarchy.

EDOLOGY and soil ecology were born at the mous diversity of invertebrates and microorgan- Pend of the 19th century with seminal books ism communities focussed their research mostly by Miiller (1887) on humus types,Darwin (1881) on classification, basic biology and ecology of on ecology, and Dokuchaev (1889) soil organisms. This per'iod culminated with on soil genesis. Biologists faced with the enor- the publication of several syntheses on the biol- ogy of soil microorganisms and invertebrates (e.g., Kiihnelt 1961; Burges and Raw 1967; Laboratoire d'Ecologie der Sols Tropicaux, Univerriti Parir WIRD, 32 rue H. Varagnat, 93143-Bondy Cedex, France. E-mail:[email protected] Dommergues and Mangenot 1970). The next

73

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." ,-.._ _-.-..i-. -. ,,,. .. . .<..*..,. II,.. ,I ,_:.. ,,,. <,.. ...' . _-. ,;,, '.' ; ...... - . . '' ... . . , ... ,. .., . . . ' .. .. :: ...... 74 LAVELLESOIL SCIENCE decade was dominated by the production of considers physical, chemical, and biological enormous datasets on communities of soil mi- processes and their interactions. croorganisms and invertebrates and their energy The purpose of this paper is to assess pro- budgets as part of the International Biological gresses and trends in soil ecology in regard to the Programme (Petersen and Luxton 1982).In most needs and requirements of general science, soil cases, the direct participation of invertebrates to science in particular, and the needs of societies. C mineralization was estimated to be well below Past achievements are reviewed and recent inte- 5 to 10% of the total flux, the remaining 90 to grative concepts are detailed. Their adaptation to 99% being released by microbial respiration. the needs of society and their perceptions by At the same time, Swift et al. (1979) produced users are discussed. a remarkable synthesis on decomposition SOIL SCIENCE, SOIL ECOLOGY AND processes as perceived through the large datasets THE GREEN REVOLUTION(S) published by this time. Bridging with biology, this book laid the ground for new Soil science has always provided the main research questions aimed at developing the para- theoretical background for the scientific devel- digm that decomposition, as with every process opment of practices (Pedro 1997). This in soil, results from interactions among biologi- has been the major-if not only-field of appli- cal, physical, and chemical components. Bal cation until recently, at times when other services (1982), on the other hand, using a micromor- provided by soils (e.g., moderation of water cy- phological approach, drew attention to the re- cling, shelter for seed banks, retention and release markable effects of soil organisms on soil struc- of nutrients to , decomposition of organic ture, thus linking physical processes to chemical wastes, and recycling of nutrients and regulation and biological processes of soils; the concept of of earth's major element cycles) were not ac- ecosystem engineering proposed by Jones et al. corded the importance they are now. The green 1994 had already been considered in these early revolution that has developed during the past studies, which showed that biogenic structures four decades has allowed us to face the highly produced by invertebrates or microorganisms challenging goal of duplicating food production (e.g., earthworm casts and galleries, fe- in less than 30 years and improving per capita cal pellets, microbial colonies) comprise a some- food availability in many countries (FAO 1995). times large proportion, if not all, of the aggregates This objective has been met by increasing culti- and macropores dealt with by soil physicists. Pre- vated areas and the use of fertilizers and pesti- sent soil ecology is the result of the convergence cides, selecting increasingly performing cultivars, of these three main approaches. and improving the physical preparation of soils During these early phases of development, by tillage, irrigation, and antierosive devices. . . soil ecology has used mainly concepts and para- During this period, soil classifications have digms borrowed from other disciplines, and its been developed and used largely to identify the influence on and ecology has been soils best adapted to novel agricultural techniques rather limited, as reflected in the low importance ( Staff 1975; Duchaufour 1977). Al- given to soil ecological issues in most textbooks though some would address the question of agri- of soil science and ecology and the preference of cultural use directly (e.g., FAO 1978; Sanchez et soil ecologists to publish in their specific discipli- al. 1982), doubts have sometimes been expressed nary journals. This trend is being progressively about the zeal adaptation of this knowledge to reversed by the formulation of new challenging the needs of societies (Duda1 1986). Studies on concepts that propose novel views of soil fun& the chemical fertility of soils and on agricultural non and ecological processes in review articles machinery and its physical impact have also ac- (Coleman et al. 1983; Lavelle et al. 1993; companied this phase (Henin et al. 1960; Seta et Ohtonen et al. 1997; Beare et al. 1995; Wardle al. 1993; Frede et al 1994.; Cannell and Hawes and Giller 1996; Brussaard et al. 1997; Silver 1994; Keicosky and Lindstrom 1995;Entry et al. 1997; Andren et al. 1999) and textbooks 1996; Papendick and Par? 1997). The needs of (Coleman and Crossley 1996; Lavelle and Spain plants for fertilizers and the efficiency of their 2000). This dynamic is supported by the recog- use have been explored thoroughly to provide nition that practical solutions to environment adequate fertilization in sometimes highly inten- problems linked to soil use and the maintenance sive crops (see reviews by Newman 1997 and of ecosystem services provided by soils (Daily et Magdoff et al. 1997). al., 1997) clearly need a systematic approach that The major inputs of biology during this phase I

VOL. 165 - No. 1 ECOLOGICALCHALLENGES FOR SOIL SCIENCE 75

have concerned the relationship between plants control and manipulation of these almost univer- and the organisms that interact directly with them. sal symbionts of plants is still limited. Control of parasites, mainly through direct chem- At the' beginning of the 199Os, reports ac- ical attacks, has grown very rapidly,leading to a sit- knowledged the spectacular results of the combi- uation where control is reasonable in many in- nation of direct interventions (FAO 1995). They stances; however, the cost is a sometimes huge also pointed to the rapid spread of environmental applicvion of a large number of at rela- problems that now require solutions to meet the .. . tively short intervals and the continuous creation continuous challenge of feeding more people un- . 1. of new molecules as pests adapt to the currently til human populations finally stabilize.As new land ". applied products. There have, however, been some to cultivate becomes increasingly rare, soils under crisis situations in which excessive and inappropri- cultivation are facing significant physical and ,. ate use of insecticides has resulted in a decline in chemical degradation while pollution of water ta- production (Ooi et al. 1992). Although some bles, eeshwaters, seashores and littoral areas, and progress has been made in the selection of increas- atmosphere is progressing at alarming rates, espe- ingly selective molecules, nontarget effects remain cially in countries where intensification has been significant for a large number of substances in use, maximum. A new approach to agriculture, called and their transfers to other parts of the ecosystem the second paradigm, has been proposed: rely and landscape and persistence in the environment more on biological processes by adapting germ- is a matter of real concern. Of major concern is plasm to adverse soil conditions,enhancing soil bi- the effect of nematicides and füngicides, which ological activity, and optimizing nutrient cycling have had side effects such as the drastic reduction to minimize external inputs and maximize the ef- .... ,

of and other usefil invertebrates in ficiency of their use (Sanchez 1994). It is recog- 1.. intensive annual crop systems or industrial crops nized increasingly that soils can provide a wide such as Banana or tea garden plantations (Senapati range of ecosystem services; the production of et al. 1994). Finally, the burning debate of the food and fiber is still considered the most impor- soundness of selecting genetically modified plants tant, but it is not soil's only purpose (Daily et al. resistant to specific herbicides shows clearly that 1997; Tinker 1997), and the maintenance of soil there is an urgent need to reassess the approach to quality has become a serious issue, leading to the pest management. Research in biological pest development of systems of soil survey in a large management has involved natural microbial and number of developed countries, Issues such as the invertebrate enemies of pests as part of biological role of soils in or as reservoirs control strategies. Some rather spectacular suc- of biodiversity have come to the fore, and their cesses have resulted fiom this research, which is study requires holistic approaches. Scales at which .- LI progressively associated.with chemical approaches soils are considered hpe become extremely di: , into integrated pest management (Waage 1996). verse (Wagenet 1998;Lavelle and Spain 1999). Usefül organisms have also been studied to find ways to optimize their activities in the con- DEVELOPMENT OF SOIL ECOLOGY text of highly intensive practices. The field of ni- At the confluence of soil science and ecol- trogen fixation has expended huge efforts to ogy, soil ecology has made its way to become a identify and classify microbial N-fixers and iso- truly interdisciplinary field of scientific innova- late the Nif-gene responsible for this fixation tion with proper concepts and theories. .... I . ':. . (Sprent and Sprent 1990). Until recently, ecologists borrowed con- . .. ;.. soil .. .. . At a more practicil level, techniques for inoc- cepts and theories €-om other scientific fields. It ,. u1atio.n of legume roots by locally existing or in- soon became evident, however, that important is- .. troduced strains have been developed. There have sues of soil ecology would not fit into existing been significant improvements in legume growth, models or paradigms or provide counter examples and N fertilization based on the use of legumes as to currently admitted laws. The excessive impor- green is developing in favorable circum- tance given by current theoretical ecology to an- stances; certain prokaryote- associations can tagonist relationships (predati04 parasitism, or . ... routinely fix up to 200 kg N ha-' per cropping competition) rather than mutualistic ones and the .. ..'. cycle and sometimes more (see e.g., Rinaudo et relatively little importance given to the quality, and al. 1983; Toomsan et al. 1995). On a world-wide not only the quantity, of food resources as deter- basis, an overall estimate for biological N-fixation minants of these relationships have been empha- is 10j Mt per year (Sprent 1984). Similar research sized (Swift et al. 1979; Lavelle 1983; Price 1984). have been done on mycorrhizae, although the The foodweb approach to explain ecosystem fünc-

,. ; ,/,:1...... ,,,,,-,. ,, . ...:- , ,...,. . :, . - .. 76 LAVELLESOIL SCIENCE tioning, widely developed in freshwater systems, position depends on three elements: (i) organisms has been extended ,iYith some success to soils (O),(ii) soil physical conditions (P) including cli- (DeRuiter et al. 1993; Hunt et al. 1987). This ap- mate and bedrock effects,and (iii) resource qual- proach, however, seem to reach its limits with ity (Q,i.e., the chemical quality of organic mat- large organisms (ecosystem engineers, Jones and ter produced by plants and the network of Shachak 1994) with strong indirect,nontrophic in- consumers and decomposers. Human activities fluence on other organisms present (Moore et al. were also included as a major effect in these in- 1993; Anderson 1993; Wardle and Lavelle 1997). teractions. It was then recognized that these de- The difficulty of relating biodiversity in soils terminants are hierarchically organized since fac- to soil processes is another indication that all tors operating at large scales of time and space species of soil invertebrates are far from being constrain factors that operate at smaller scales functionally equivalent. Soil systems seem to be (Lavelle et al. 1993; Beare et al. 1995; Wagenet an excellent way to address the important issue of 1998.; Izac 1994). Determinants that operate at the relationship between biodiversity and ecosys- the largest scales (i.e., climate and soil properties) tem function (GiUer et al. 1997; Brussaard et al. constrain those that operate at smaller scales, i.e., 1997; Freckman-Wall et al. 1997 ; Wardle and the plant community that determines the quality Lavelle 1997 ;Hopper et al., in press). and quantity of organic inputs to the soil, Soil ecology is instrumental to the sustain- 'macroorganisms' (= macroinvertebrates + ability of land use practices because solutions to roots) and microorganisms. However, feedback problems of maintenance of and sus- (or bottom-up) retroactions do exist, with deter- tainable production are necessarily global. The minants at lower levels of the hierarchy influenc- success-and problems-of conventional inten- ing upper levels. Furthermore, this hierarchy is sive agriculture as practiced at its peak has come potential and may not be My operational lo- from the improvement of each of the individual cally: when climate is not constraining (e.g., in elements assumed to increase production in a the humid tropics), when soils have no min- largely reductionist approach. A system approach erals such as smectites that strongly influence mi- is now needed to address these elements jointly crobial activities through several mechanisms, as compartments that interact as a global model. and when the organic matter produced is uni- One such model of crop production would heed form and decomposes easily, microbial activity closely the relationship between nutrient input may be regulated primarily by macroinverte- and uptake by plants to prevent losses to water brates (earthworms and termites) via the bio- and air (Myers et al. 1994); the conservation of genic structures that they create (Blanchart et al. through proper management of or- 1997). The adoption of this model allowed us to ganic matter inputs and macroinvertebrate and consider jointly factors that had previously been root activities; and the effects of the different al- addressed in isolation and to identify the factors I locations of land to crops and plant covers, in- of greatest importance. cluding, in some cases, non-crop plants (Hogh- This is an important step in understanding Jensen 1998; Lal 1997). questions such as the apparent contradiction be- tween soil zoologists and soil scientists in regard Concepts arid Models to the assessment of invertebrate activities. When the former provided increasing evidence that soil New concepts and models have been pro- invertebrates had a dramatic influence on the posed during the last decade that will support rites and spatiotemporal patterns of processes holistic approaches and serve as a basis for inte- soil (Anderson et al. 1985; Seti% et al. 1991; Martin grated models that will simulate the function of 1991;Blanchart et al. 1997),the latter would pro- agricultural practices of the next generation. duce models that simulate the same processes without making any mention of soil inverte- Scales and hierarchies brates (see e.g., Parton et al. 1983; Smith et al. The first question faced by ecologists was 1998). At the scale considered by these models, that of integrating determinants of soil processes hot spots of invertebra& and root activities are into a single comprehensive model. Soil scientists actually diluted in a soil volume that comprises a have long recognized that soil formation and majority of almost inactive sites (Anderson function proceed from interactions among cli- 1993). Furthermore, the same factors that deter- mate, bedrock, and living organisms. Swift et al. mine invertebrate and root activities may also (1979) then developed the concept that decom- regulate microbial activities.As a result, the inter- VOL. 165 - No. 1 ECOLOGICALCHAI,LENGES FOR SOIL SCIENCE 77 mediate action of macroorganisms is regularly 1991, Barois and Lavelle 1986; Lattaud et al. I undermined or misunderstood, even when their 1996). .-. effects are implicitly contained in some basic soil Macroorganisms have been classified into parameters that they influence in the long term, three categories,depending on the type of trophic such as C:N ratios, pH, or bulk density. For ex- relationships they have with microorganisms and ample, soil bulk density, which is influenced on the biogenic structures they may produce greatly by macrofaunal activity and dynamics, is through their mechanical activities in the soil considered constant in the CENTURY model of (Lavelle 1997). The smallest, the , nema- _.- SOM dynamics, one of the highest performing todes,and other microfauna that live in the water- . '. models in this area (Parton et al. 1988).Problems filled soil pores, are micropredators of microor- . .. arise when perturbations of invertebrate com- ganisms and do not create any structures. Of a munities affect soil physical properties and SOM larger size, the nonsocial and small dynamics that could not have been predicted by Oligochaeta Enchytraeidae are litter-transformers models, especially when they cannot take into that produce organic biogenic structures in the account temporal changes in soil bulk density or form of fecal pellets. These structures, which C:N ratio. serve as incubators for microbial digestion before Soils also present a hierarchical physical and they are reingested, do not usually last long. They spatial organization, as emphasized in the early may alter the timing and spatial patterns of de- synthesis of Tisdall and Oades (1982) and refined composition, but they have limited impact on soil further with the introduction of fractal models physical properties (Hanlon and Anderson 1980). and the efforts made to explore spatial hetero- Soil ecosystem engineers are mainly termites, geneity at different levels using spatial statistics ants, and earthworms, which conduct important (see e.g., Bartoli et al. 1993). Nowhere in the mechanical activities and produce organo-min- ecosystem has heterogeneity been better assessed eral biogenic structures. These are solid structures than in soils. This approach has helped to define that may persist much longer than the organisms the levels at which soil processes should be stud- that produce them, and they affect the dynamics ied. At these levels, functional domains of a par- of SOM and soil physical processes significantly ticular category of organisms, defined as 'ecosys- (see Elkins et al. 1986; Mando and Miedema tem engineers', have been identified by 1997; Folgarait 1998; Villenave et al. 1999; ecologists and become the scale at which inter- Blanchart et al. 1999).Through the modifications disciplinary approaches have largely developed of the environment and changes in resource avail- (Lavelle 1984;Jones et al. 1994;Beare et al. 1995; ability that they promote, soil ecosystem engi- Lavelle 1997; Lavelle et al. 1997; Beare and neers influence the composition and activity of Lavelle 1998) the smaller organisms- (ir th li

tional importance) that inhab il Interactions betweeti nzicro- atzd nzacroorgataisms: The compete with them for, e.g., surface leaf litter I Sleeping Beauty arid the Ecosystenr Eigineers (Marinissen and Bok 1988; Loranger et al. 1998; I! Microorganisms are responsible for more Decaëns, 1999). II than 90% of the mineralization that occurs in soils (IBP); they are capable of decomposing any Ftltzctiotzal doniains in soils kind of natural substrate and multiply in short Functional domains are parts of the soil that periods of time, sometimes in a matter of days. are influenced by a major biotic or abiotic regu- The turnover time of their biomass, however, lator. They are recognizable in a set of structures .... generally varies fiom 6 to 18 months, which in- (pores, aggregates, fabrics) generated by the reg- .. dicates that they are inactive most of the time. ulator that can be physically separated fiom the . .. This apparent contradictory observation is soil matrix (Fig. l)(after Beare and Lavelle 1998). named the Sleeping Beauty Paradox (Lavelle et They are colonized by rather specific communi- I al. 1995).The Prince Charming of the story are ties of microorganisms, other invertebrates, and, macroorganisms and other physical processes that possibly, roots. They are places where basic : I, II bring microorganisms into contact with new processes of soil fùnction operate at specific spa- substrates to decompose. Macroorganisms, in tial and temporal scales. '1 turn, are known to have limited proper digestive Every structure existing in soils is part of a abilities and rely largely on the ability of mi- functional domain. Some functional domains croorganisms to digest a wide range of substrates may be closely related, however, and their fio for them (see e.g., Slaytor 1992; Rouland et al. tiers difficult to identify with precision. ..

LAVELLESOIL SCIENCE ’ -

REGULATOR image analysis or 3D tomography, has proved to . be an efficient tool for classifying and quantify- x ing biogenic structures accumulated in the soil ROOTS X (e.g., Lamparsky et al. 1987; Chadoeuf et al. X x 1994; Binet and Curmi 1992;Jegou et al. 1998). TERMITES x IERMTOSPHERE

(X X Comniirnities PLANTS x) UTlERSYSEhl Soil ecosystem engineers and abiotic regula- (X X x 7 EARTHWORMS] DRILOSPHERE tors create specific conditions of physical envi- ronment and resource availability in their func- (x x ANTS 1 X ) MWMECOSPHERE tional domain. As a result, specific communities of organisms from subordinate groups (litter transformers and micropredators) are established in these domains. They form foodwebs, the ’ composition and energy inputs of which are de- STRUCTURES termined by the activities of the regulator. f Fig. 1. Functional domains in soils (note that a vertical Processes rather than a horizontal separation of items leads to definition of the porosphere and aggregatesphere Most processes that operate in functional do- t (Coleman and Crossley 1996) and soil foodwebs, re- mains are not specific. This is the case for all the spectively). transformations linked to C and for nutrient cy- cles that follow the same pathways and are per- formed by the same microorganisms everywhere Regulators in the soil. Conversely, other processes may be Regulators may be biotic or abiotic. Ecosys- considered highly specific. This is the case for tem engineers such as earthworms, termites, or fluxes of energy and matter across foodwebs and ants create their own functional domains, i.e., the priming effects on microbial activities resulting drilosphere, termitosphere, and myrmecosphere, from the production of specific resources such as respectively. Plants create two Werent spheres of exudates or mucus in especially active microsites influence in soils, the rhizosphere of roots and such as the rhizoplane of roots (i.e., a volume ap- the litter system formed by the accumulation of proximately 1-pm thick, in contact with the root dead leaves and shoots. Biotic functional domains surface) or the guts of termites or earthworms are synonymous with the “biological systems of (Tenkinson 1966;Lavelle and Gilot 1995). regulation” described by Lavelle (1984). Abiotic regulators may also create sets of recognizable Scales structures;this is the case for fi-eezing-thawingal- Functional domains are places where basic ternations that create mosaic patterns in soils, or processes of soil finction operate following spe- drying/wetting cycles that produce considerable cific spatial and temporal patterns. Processes such bioturbation and the formation of cracks in soils as organic matter decomposition may be alter- with swelling clay minerals. nately enhanced or inhibited, depending on the scale of time and space at which they are consid- Stnictrrres ered. For example, in the drilosphere (the func- Functional domains comprise a set of pores, tional domain of earthworms), mineralization is aggregates, and fabrics that have been accumu- greatly enhanced in the gut and fi-esh globular lated by the regulators. They can be described casts, that is to say, in a definite number of small and classified in isolation or at the scale of the hot spots, during periods of hours to days; in ag- whole domain. Biogenic structures considered as ing casts (which may represent hundreds of tons of extended phenotypes of species (Dawkins 1976) aggregates) mineralization is almost nuWied as are microsites where taxonomic diversity may in- long as the casts retain the$ structure, which fluence functional diversity (Lavelle 1996a). A means time scales of months to years (Lavelle new research approach aims at classifying them 1997).At larger scales, the overall effect of earth- into homogenous groups and relating their phys- worm depends on the balance between short- ical and chemical properties to measurable effects term stimulation and longer-term protection. The on specific soil processes (Lavelle et al. 1997; drilosphere, as with any other functional domain, Decaëns 1999).Micromorphology, coupled with may still exist’and regulate soil processes several VOL. 165 -No. 1 ECOLOGICALCHALLENGES FOR SOIL SCIENCE 79 years after the earthworms have been eliminated of determinants that influence the quality and (Lavelle et al. 1997).This puts new light on the is- amount of available organic resources, as suggested al. sue of the dynamics of aggregation in natural and by the hierarchical model (Martin et 1991; managed ecosystems, indicating it is influenced Tayasu et al. 1997; Chen and Wise 1998). Experi- much more by invertebrate actjvities than cur- ments and field observations using isotopic meth- rently thought. ods constitute an efficient approach to this problem. The functional significance of biodiversity in NEW CHALLENGES FOR soils has been identified as a major scientific con- SOIL ECOLOGY cern given the present threats to Parts of the conceptual bases of soil ecology are (Freckman et al. 1997). Another question relates still rather new and need to be refined as their use to the relationship between above- and below- generalizes. Some present questions of ecology ground biodiversity. This question has beemnow need to be addressed in the context of This is discussed, and research hypotheses have been for- soils. al. the case for the effects of hgmentation on soil mulated (l3russaard et al. 1997; Hooper et in biota communities and populations at local and re- press) (Fig. 2). gional scales. Interactions among soil biota still of- Answers to some of the questions challeng- fer vast opportunities to check the importance of ing soil science should benefit fiom recent devel- negative (i.e., predation, parasitism, and competi- opments of soil ecology. Modeling SOM dy- tion) relationships compared with mutualism. An- namics has been a great challenge during the last other important question is the control on process two decades, and considerableprogress have been rates via foodwebs: are rates regulated by higher made; there is still scope for some improvements level organisms in the (i.e., by predators of predictions and an explicit integration of bio- al. in a top-down array of determinants) or by a suite logical activities (Smith et 1998).

Diversity of primary producers Chemical -diversity ofstructural f composition compounds -novel defense

compounds C resource ~ ___j ..._- - " - phenology - rooting structure C Resource Distribution in time h ete rog e n e ity x Distribution Intermediate selectivity-feeding of in space stress Hyp. -environmental Diversity 1 .. of etritivores Trophic interactions I Selectivity of predators in detrit. - . foodweb .. Cc"etition among lo Diversity of other predators components Selectiv of the detrital food ^C.

Fig. 2. Mechanisms that link above-groundand 80 " . . LAVELLESOIL SCIENCE

I Finally, accurate studies ,of the, dynamics of lapsed and formed a 5-cm impermeable crust soils using methods and approaches of soil ecol- that created severe limitations to plant growth ogy are likely to provide rather surprising results (Chauve1 et al. 1999). Hydromorphy developed in the near füture. For example, recent studies below the crust and extended 1 to 2 min depth, have shown how trees may transfer silica from thus changing the entire soil profile in as little as deep soil horizons to surface layers through the 3 years. During this time, the direct consumption absorption of this element by roots, transfer to of organic matter by the earthworms and other the leaves, and release in decomposing leaves unidentified mechanisms (possibly methaniza- (Lucas et al. 1993). This view, in contradiction to tion) decreased SOM stocks by 18 t/ha in the the classical theory of a progressive loss of this el- upper 20 cm of soil. Such events, identified as ement by during soil aging, emphasises biodiversity accidents, may occur more fie- the possible strong,bottom-up effects of biota on quently than is normally expected. The pullula- soil properties in some conditions. The Gaian tion of ant nests following abandonment of view of soils and the planet as homeostatic sys- paddy rice fields to natural fallow in northeast tems regulated by biological activities is finding Argentina is another example of a drastic change some support in these results (Lovelock 1993; in soil profile occurring in a very short time Lavelle 1996b).Another example comes from re- when communities of soil invertebrate engineers cent studies based on micromorphological ap- are disturbed (Folgarait et al. 1998). Interestingly, proaches revealing that, in many soils, most ag- a disturbance as large as the one observed in the gregates are formed by invertebrate engineers. Amazonian soil may revert rapidly when the soil Because they are biological structures, they have compacted by the activity of a dominant com- sometimes surprisingly rapid turnover, and this pacting species is re-exposed to the original in- explains why soil attributes sometimes consid- vertebrate community (Fig. 3). ered to be rather stable may, in the long term, These fundamental research questions are es- change at short notice. For example, this is the sential if we are to address larger issues, e.g., the case for soil macroaggregates when changes in modeling of SOM dynamics or changes in hy- invertebrate communities occur. Disappearance draulic soil properties, or understand the bases for of the invertebrates that produce stable aggre- sustainable production of agroecosystems and the gates interrupts the production of new aggre- effect of land use practices. The composition and gates, and soil aggregation is changed as aging ag- diversity of soil microorganisms and invertebrate gregates progressively collapse. In another case, communities is certainly influenced by a wide this one reported in Central Amazonia, a com- range of factors that operate at different scales of pacting earthworm species, Pontoscolex corethru- time and space. Fragmentation of space, colo- rus, invaded a pasture cleared from the primary nization abilities of organisms, and their toler- forest and produced an excessive amount of large ance to different types and intensities of distur- casts. Because these casts were unstable, they col- bances are essential attributes of populations in

Porosity % Dense compacted areas % 35 I 6oi 28- 21-

14- 7-

0- 0- 0- Forest Pasture Forest Pasture

Fig. 3. Changes in the proportions of soil porosityx and dense areas (identified as earthworm casts) measured on thin sections of soil in monoliths (25 X 25 30 cm) 1year after their transplantation from a forest with a diverse the endogenic earthworm, Pontoscolex corethrums (o), and vice ver VOL.165 - No. 1 ECOLOGICALCHALLENGES FOR SOIL SCIENCE 81

this regard. Understanding the relationship be- of and profit. Great importance is tween the diversity of plants and soil biota d given to biogenic structures, i.e., the organo- also provide essential information for predicting mineral structures and voids produced by soil in- the impact of management options on the com- vertebrate engineers, as components of the soil position and activities of invertebrate and other structure that promote suitable properties for organism populations. plant growth and also as indicators of inverte- At the next level, it is important to relate the brate activities.In the long term, invertebrate ac- composition and abundance of communities to tivities may be absent during given periods of their effects on physical processes, SOM, and nu- time on parcels of a given size when required by trient cycling, their intensity, and persistence in production constraints. Under such conditions, time. A clear understanding of these mechanisms monitoring the soil physical structure, especially is necessary to design management practices that the biogenic structures produced by macroin- optimize biological activities and improve the vertebrates, would allow us to determine when sustainability of the system. Models used to pre- the inherited physical effects attributable to past dict the effect of practices will consider various invertebrate activities no longer exist. Different scales of space and time, including the cultiva- management practices would then be applied to tion plot, farm and/or catchment, and region. create suitable conditions for invertebrate activ- An example of a conceptual model of that sort ities and improve soil conditions. The great chal- is given in Fig. 4 (Mariani, unpublished data). lenge is to have accurate indicators to evaluate This model explains the interactions between soil conditions and favorable conditions for fast the agrosystem (i.e., the sum of management op- colonization of the plot. This means that diverse tions chosen), soil attributes (mainly SOM dy- and abundant populations are available in plots namics and physical structure), and soil macro- adjacent to the area opened to recolonization . The aim is to use this model to develop and that new conditions present in the plot are practices that maintain diverse macrofaunal ac- suitable to attract migrants and to allow rapid tivities at an optimal level to take advantage of growth of their populations. Finally, a number of their short- and long-term beneficial effects on other ecosystem services provided by soils will soil physical structure and SOM dynamics while come to fruition using the concepts and models meeting the requirements of the farmer in terms that are currently in development.

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MACROFAUNA-8, I , A Fig 4. conceptual model of the type use? to pr ices. 82 LAVELLESOIL SCIENCE

SOIL ECOLOGY ATTITUDES ments will be better 'established and processes TOWARD ENVIRONMENT leading to losses (NyP, CO,, methane) better AND DEVELOPMENT ISSUES understood. Management of organic matter is now considered as essential in any system (fer- In a way, ecology may be considered the ac- tilisers are better used in the presence of OM) countancy of natural systems. Ecosystem research and the maintenance of soil invertebrate engi- studies energy fluxes and nutrient and matter c , ;. . neers is necessary for long term conserva- , *.a . soil .: ,. budgets. Every loss in elements, decrease in . ., tion. Systemic approach is able to identi@ the .. process rate or species richness or physical degra- .... exact trade off among the dflerent constraints: .,". dation is intuitively considered to be negative. production and financial sustainability, environ- ,. Managed ecosystems always look highly imper- ,, ment protection and . As sci- .. fect compared with natural ones, which tend to ence progresses the uncertainty on processes serve as references for future improvements of that gives space to political interpretations is artificial systems. The ecological perception of narrowing. .. ecosystem functioning has sometimes generated . .. contractive reactions and exaggeratedly conserva- PUBLIC INFORMATION AND tionist points of view in the face of the poor TRAINING IN SOIL ECOLOGY ecological quality of most agroecosystems. An .. opposite point of view is supported by agrono- Society in general and farmers as well are fre- .. mists, who look for more artificialization and quently ignorant about the role played by soil ." . '. .'-. simplification of the system and evaluate their biota. In a survey of 163 farmers &omthe state of . ,...... i , practices in terms of productivity and profit rather Vera Cruz (Mexico), 55% ignored the effect of than aesthetic or environmental considerations. earthworms on soil fertilitj-, 31% recognized .,.. Ecologists are continuously integrating view- their beneficial effect, and 11% considered them . '. points from economics and the social sciences harmful, mainly because they mistook them for I. and consider the issue of sustainability at levels intestinal parasites (Ortiz et al. 1999). Further- fiom water catchments to villages or regions. more, in Congo, where the traditional maala sys- This new trend is logically derived from the nat- tem is one of the few annual cropping systems ural enlargement of levels considered as research that enhances earthworm activities, farmers do progresses. International programs have been in- not seem to be aware of this effect, nor do they strumental in elaborating comprehensive ap- acknowledge the importance of soil invertebrates proaches that set human needs and constraints at to . This ignorance, with some no- the center of research approaches. This has been table exceptions, is surprisingly deep rooted in the case, for example, in programs developed by mythologies and cultures. Societies tend to fear UNESCO (Man and the Biosphere) and by insects and to undermine earthworms. This ex- IDS in its Decade of the Tropics, such as the plains why practices aggressive for soil biota and Tropical and Fertility (TSBF) pro- the environment have, until recently, developed gram (Swift 1986 ; Swift and Woomer 1994). with no limits. However, this trend has been accelerated greatly However, these environnient-unfriendly by donors who favor direct development and ap- practices have led to crises and threats that give plication of research at the farm level through the space to new technologies. Mad cow disease, development of participative research. Increasing fears and fights against GMOs by Indian farmers .. difficulties in maintaining research centers and and consumer unions, and diosin in Belgian . , .". .. the relatively poor efficiency of transfer to farm- chickens have created interest in ecological tech- .. . .. ,. ers has accelerated this trend. This has led to bet- nologies based on the use of earthworms and or- ter consideration of the knowledge of farmers ganic wastes that have been largely emphasized . .. and other soil users, which may be compared by newspapers in Europe and worldwide. Early with scientific results and/or serve as a basis on findings on soil problems caused by lack of di- which to build. versity have also had large +acts. The effect of As awareness of the implications of soil use invasive earthworms on soil degradation inAma- on global environment is growing, scientific zonia (Chauve1 et al. 1999) and the development evaluations of their function using Ecological of new technologies using earthworms to com- approaches is needed. As soil function is better post domestic wastes (Edwards and Neuhauser understood, minimal rates for processes (ex. 1988) or regenerate degraded soils of tea garden renovation of soil aggregates, maintenance of plantations (Senapati et al. 1999) have been ) will be identified, budgets for ele- widely advkrtised.

.. VOL. 165 No. 1 - ECOLOGICALCWLENGES FOR SOIL SCIENCE 83

CONCLUSION . Lawton (eds.). Chapman & Hall, New York, pp. 94-106. In an opening lecture at the last ISSS Con- Anderson,J. M., M.A. Leonard,P. Ineson, and S. Huish gress at Montpellier,Swift (1998) stated:"Soil sci- S:1985. Faunal biomass: A key component of a ence has been brilliantly informed by reduction- general model of nitrogen mineralization. Soil ist physics and chemistry, poorly informed by Biol. Biochem. 17:735-737. biology, ecology, and geography, and largely un- Andrén, O., L. Brussaard, and M. Clarholm, 1999. Soil informed by the social sciences." This sets the organism influence on ecosystem-level processes- ground for the present and future need to further by passing the ecological 'hierarchy? Âppl. Soil expand interdisciplinary research to face the ma- Ecol. 11:177-188. Bal, L. 1982. Zoological ripening of 1. The con- jor problems posed by soil use. Past experiences soils. have shown clearly that interdisciplinary research cept and impact in pedology, forestry, and agricul- I. . ture. 2. The process in two under develop- requires specific interdisciplinary methods and two ing forest in a recently reclaimed Dutch polder. concepts. In the last decades, soil ecology has Pudoc, Wageningen,The Netherlands. participated actively in the development of sys- Barois, I., and Lavelle P. 1986.-Changes in respiration temic approaches to soil science. There is still rate and some physicochemical properties of a much room for improvement in the concepts tropical soil during transit through Pontoscolex and models thus created The next challenge corethrrrnis (Glossoscolecidae, Oligochaeta). Soil seems to be to integrate adequately economic Biol. Biochem., 18 (5) 539-541. and sociologicalparameters in models of soil use; Bartoli F., G.Burtin,R. Philippy, and E Gras. 1993. In- this means adapting scales at which soil science fluence of fir root zone on soil structure in a 23 m approaches functions to those that matter to in- forest transect: The fractal approach. Geoderma 56 67-85. dividual users and/or to the society (Izac 1993). Beare, M., and P. Lavelle. 1998. Regulation of micro- .i . Another great matter of concern is the rather un- bial activity and organic matter dynamics by ' .,. .!#. . satisfactory transmission of knowledge to stake- macroorganisms:Integrating biological function in holders and practitioners. The approach of soil soil. In ISSS Congress, Symposium no. 9, Montpel- scientists concerned with this problem (Ruellan lier (CD-Rom). 1994) should be supported better in order to ac- Beare, M. H., D. C. Coleman, D.A. Crossley, P. E Hen- celerate the implementation of the second para- drix, and E. P. Odum. 1995. A hierarchical ap- digm in agriculture, that is, to achieve a better in- proach to evaluating the significance of soil biodi- tegration of basic biological processes (Sanchez versity to biogeochemical cycling. Plant Soil 170: 1994), to reach this next paradigm, which will 1-18. Binet, F. and P. Curmi 1992.Structural effects of Lum- reconcile the ecological and economical sustain- bricus terrestris (Oligockaeta Lirtdxicidae) on the ability of soil use. The contribution of soil ecol- soil-organic matter system: Micromorphological ogy will be to design better artificial systems for observations and autoradiographs. Soil Biol. the management of natural processes and the in- Biochem. 24: 1519-1 523, vertebrates that have built soil fertllity for ages. Blanchart, E.: A: Albr'echt;J. degre,-A. Duboisset, B. Pashanasi, P. Lavelle, and L. Brussaard. 1999. Effects ACKNOWLEDGMENTS of earthworms on soil structure and physical prop- This paper has benefited enormously from erties. Itt Earthworm management in tropical agroecosystems. P. Lavelle, L. Brussaard, and P. discussions with scientists with many years of soil Hendrix (eds.). CAB International, Wallingford, experience in various disciplines who will cer- UK, pp. 139-162. tainly recognize their influence in these pages. 1 Blanchart, E., P. Lavelle, E. Braudeau, Y.Le Bissonais, am especially grateful to the TSBF (Tropical Soil and C.Valentin. 1997. Regulation of soil structure Biology and Fertility) program, which has been a by geophagous earthworm activities in humid sa- unique place for developing and trying new ideas vannas of Cote d'Ivoire. Soil Biol. Biochem. and concepts, to Armand Chauve1 his comments 29:431-439. on early drafts of this paper, and to Roger Schae- Brussaard, L., V. M. Behan-Pelletier, D. Bignell, V. K. fer for reading the proofs. Brown, W. Didden, P. Folgarait, C. Fragoso, D. W. Freckman, V. S. R. Gupta, T. Hattori, D. Hawksworth, C. Klopatek, P. Lavelle, D. W. Mal- REFERENCES loch,J. 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