ecology of plant and free-living nematodes in natural and ...dneher/publications/corrected...

PY48CH18-Neher ARI 5 July 2010 19:32

Ecology of Plantand Free-LivingNematodes in Naturaland Agricultural SoilDeborah A. NeherDepartment of Plant & Soil Science, University of Vermont, Burlington, Vermont 05405;email: [email protected]

Annu. Rev. Phytopathol. 2010. 48:371–94

First published online as a Review in Advance onMay 10, 2010

The Annual Review of Phytopathology is online atphyto.annualreviews.org

This article’s doi:10.1146/annurev-phyto-073009-114439

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Key Words

ecological succession, optimal foraging, biogeography, food web,niche partitioning, ecosystem stability

Abstract

Nematodes are aquatic organisms that depend on thin water films tolive and move within existing pathways of soil pores of 25–100 μmdiameter. Soil nematodes can be a tool for testing ecological hypothe-ses and understanding biological mechanisms in soil because of theircentral role in the soil food web and linkage to ecological processes.Ecological succession is one of the most tested community ecologyconcepts, and a variety of nematode community indices have been pro-posed for purposes of environmental monitoring. In contrast, theoriesof biogeography, colonization, optimal foraging, and niche partitioningby nematodes are poorly understood. Ecological hypotheses related tostrategies of coexistence of nematode species sharing the same resourcehave potential uses for more effective biological control and use of or-ganic amendments to foster disease suppression. Essential research isneeded on nematodes in natural and agricultural soils to synchronizenutrient release and availability relative to plant needs, to test ecologicalhypotheses, to apply optimal foraging and niche partitioning strategiesfor more effective biological control, to blend organic amendments tofoster disease suppression, to monitor environmental and restorationstatus, and to develop better predictive models for land-use decisions.

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INTRODUCTION

Andre et al. (3) described soils as the finalbiotic frontier and suggested that we knowmore about outer space and the depths of theocean than we do about the soil biology of ourown backyard. This review covers advancesin nematology since 1999 that pertain to therole of nematodes in the soil and rhizosphere(103, 165). Even with recent advances and thesignificant progress discussed in this review,the knowledge gap is vast, and discrepancies inbasic ecology and biology of free-living nema-todes and soil nematodes in natural ecosystemsremain as they have for the past 25 years.Knowledge of plant-parasitic nematodes ofeconomic or quarantine importance is ordersof magnitude greater than that of free-living orbeneficial nematodes that compose up to 60%to 80% of the soil nematode community. Con-sequently, studies of free-living nematodes andsoil nematodes in natural ecosystems are severalsteps behind those of plant-parasitic nematodesand nematodes in agricultural ecosystems (53).Nematode ecologists are in initial stages ofelucidating the taxonomy and systematics offree-living nematodes in agricultural systemsand all soil nematodes in grassland, forest, andwetland systems, as well as life history strategiesand the relationships between nematodes andtheir contribution to ecosystem function (10,77). Evolutionary and geological evidencesuggests that soil nematodes have considerablylonger histories on Earth than organisms thathave received more attention, such as mammalsand vascular plants (70). This evolutionary his-tory alone suggests that they play an essentialrole(s) in ecosystem structure and function.

Soil nematodes (typically 40 μm to 1.0 mmin length) are classified either as microfauna ormesofauna; their small size makes them unableto reshape soil and, therefore, they are forcedto use existing pore spaces, water cavities, orchannels for locomotion within soil. Most ne-matodes inhabit soil pores of 25–100 μm di-ameter. Nematodes depend on water films (1–5 μm thick), which coat and surround soil par-ticles, to move through the soil system (61).

The hierarchical and heterogeneous soil struc-ture gives rise to a complex distribution ofephemeral water-filled pores and films that cre-ate many unique microhabitats. Habitable porespace, that is of sufficient size and connectiv-ity to support nematodes, accounts for a smallportion of total pore space (67). Within thehabitable pore space, nematode activity is influ-enced by the balance between water and air (3).Saturation and drought both impact composi-tion of nematode communities in soil becausethese conditions result in anaerobiosis and de-hydration, respectively.

Definitions of Ecology

An increased public awareness of environmen-tal problems has made ecology a common butoften misused word. Ecology is the scientificstudy of the interactions of organisms with oneanother and with the physical and chemical en-vironment. Ecological studies may focus on oneor more scales: populations of a single species,an interacting community involving popula-tions of many species, movement of matter andenergy through a community within an ecosys-tem, large-scale processes within a biome, orglobal patterns within the biosphere. Researchquestions depend on the hierarchy of scale.

Several review articles have been publishedon basic biology and ecology of free-living (52)and plant-parasitic nematodes in agricultural(53, 165) and natural (35) ecosystems. Otherreviews highlight the beneficial role of nema-todes in ecological processes, including decom-position, nitrogen cycling (10, 77) and diseasesuppression (85, 135, 169). One of the first com-prehensive reviews of agricultural and naturalecosystems was prepared by the Polish nema-tologist, Lucyna Wasilewsa (159). Since then,comparative reviews have been published (103),and ecologists have begun to study diseases innatural ecosystems. Relatively well-studied nat-ural systems are grasslands, coastal dune sys-tems, and forests. This review focuses on theecology of plant-parasitic (or root-feeding) andfree-living nematodes that complete their en-tire life cycle within terrestrial soils or within

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plant roots. It will not include nematodes inaquatic ecosystems (144), nematode parasites ofvertebrates, or nematodes affiliated with insectsas pathogens or mutualists (84).

Historic Perspective

Application of ecological approaches andknowledge of biological suppression of diseasein natural ecosystems is receiving more atten-tion as environmental concerns mount for thelongevity and quality of our natural resources.The field of nematology will be well served if itexpands its attention to (a) biological and cul-tural approaches to enhance the habitat and ef-fectiveness of natural enemies of plant-parasiticnematodes, and (b) the use of nematodes as bi-ological indicators of soil quality.

Broad spectrum nematicides were shown toincrease crop yields in the late 1940s and early1950s, which increased an awareness of nema-todes and increased the number of nematol-ogists employed in the United States (166).Management of soilborne pathogens has re-lied historically on application of syntheticchemical biocides. Soil fumigation with gen-eral biocides decreases microbial populationsand nearly eliminates nematodes. Fumigationof soil with general biocides results in a depau-perate soil matrix that can only be inhabitedby primary colonists. Although recovery oc-curs, population densities of beneficial soil ne-matodes may not return to prefumigation lev-els, even after five months (166). A progressionof colonization by early successional species isfollowed by more-specialized, late-successionaltaxa (42). Several effective nematicides are be-ing removed from the marketplace because oftheir impact on global climate as well as becauseof the ecological dysfunction that they trigger(56, 163). The consequences of other recenttrends in management of arable lands that callfor further research include (a) reducing culti-vation in response to loss of soil by erosion and(b) the loss of resistance genes in crops causedby strong selective pressures created by exten-sive planting of monocultures. Crop yields maydecrease unless alternative and equally effective

strategies for management are adopted. For ex-ample, biological and cultural alternatives canbe implemented to enhance the habitat and bi-ology of natural enemies.

Since 1988, there has been a tremendousincrease in the emphasis on the use of nema-todes as indicators of soil condition (52) andtheir predictive use in soil management (45).Formerly, focus in nematology was on the con-trol of parasitic and harmful species, but nownematodes are more often seen as integral andpotentially useful components of soil systems.As indicators, nematodes have advantages overother soil fauna. Protozoa may be more abun-dant but their lack of morphological charactersmakes taxonomic identification difficult. More-over, conditions for encystment and excystmentare not well synchronized with general distur-bance, suggesting that population changes maynot reflect levels of disturbance as readily as ne-matode populations (38). Although mites andcollembolans are relatively large, with abundantcharacters for taxonomic identification, and areuseful indicators in many habitats, these faunaare not always abundant in stressed and dis-turbed conditions. Complete community enu-merations that include all microinvertebratesare more laborious to extract and taxonomicallyless approachable than focusing on nematodecommunities (3). In light of these advantages,the study of nematodes is most likely to con-tribute significantly to our understanding of bi-ological processes in soil.

Ecology research spans a broad temporaland spatial scale of investigation. For the pur-poses of this review, the focus is on population,community, and ecosystem ecology, includingbasic and applied dimensions. Applications in-clude environmental monitoring, restoration,and disease management in agricultural andnatural ecosystems.

Population Ecology

Population ecologists focus on individualspecies and may ask questions regarding theinteraction of morphological, physiological,and behavioral traits, plasticity of the traits

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r-selected: life-history traits thatpromote rapidpopulation growth,e.g., small size,precociousreproduction,semelparity, a largereproductiveallocation, and theproduction of manybut small offspring

K-selected: life-history traits thatcontribute to apopulation that staysclose to its carryingcapacity, e.g., largesize, delayedreproduction,iteroparity, a smallreproductiveallocation, muchparental care, and theproduction of few butlarge offspring

Food web: energyflow or feedingrelationships in acommunity thatincludes all linksrevealed by dietaryanalysis

Evenness index:maximum value iswhen all taxa haveequal abundance in acommunity, andsmallest value when asingle taxon becomesdominant

Similarity index:ratio of the number ofcommon species foundin two communities tothe total number ofspecies that are presentin both

(83), causes and consequences of dispersal (74)and dormancy (160), outcome of life-historyadaptations (16), and/or impact of stress onpopulation structure. Population ecology con-cepts examined in nematology include density-dependent regulation of populations (53), pop-ulation dynamics (137), natural selection, andevolution. Population dynamics of nematodeshave been modeled using logistic, negative bi-nomial, stage-structured population growth,predator-prey equations, and simulation mod-eling (53).

Community and Ecosystem Ecology

Community ecologists examine interactionsbetween species or trophic groups (sometimesreferred to as guilds or functional groups),including spatial relationships and communityassembly among different species that occur inthe same habitat. Interactions between speciesinclude predation, competition, parasitism, andmutualism. At a single time point, communitiescan be described by their structure and com-position. Change in community compositionthrough time is a reflection of both seasonaldynamics (50) and ecological succession (42).Questions in community ecology addressthe dynamics of species interactions (53), therelationship between complexity and stabilityin ecosystems (91), the characterization oforganisms as r- or K-selected in relationshipto ecological succession (15), plant-herbivorecoevolution (94), and energy (carbon) andnutrient fluxes through food webs (73). In-dices of diversity, evenness, similarity, andecological succession have been used to de-scribe nematode community composition andstructure (54, 117). Goals in community andecosystem ecology include identifying sentinelor keystone taxa, quantifying the contributionof nematodes to nitrogen cycling, and defininglag effects between organisms and their impacton biogeochemical cycling (157; D.A. Neher &M.E. Barbercheck, unpublished data). Answersto these questions strengthen the justification touse nematode communities as biological indi-cators of soil quality because policy makers and

government agencies prefer indicators thatreflect ecological process and/or ecosystemfunction.

How Plants Affect Nematodes

Composition and structure of terrestrial com-munities vary among ecosystems because ofcontrasting plant composition and phenology,soil properties, and microclimates. Agricul-tural production fosters varietal selectionsfor higher yields, generating a tradeoff in theroot-to-shoot ratios that affect the quantityand quality of nutrients and energy flowingthrough soil food webs in both space andtime. Root growth is more extensive andless ephemeral in perennial plants than withannual crops and supports a soil communitywith many omnivores and predators. Soilcommunity composition with perennial cropsresembles that of natural ecosystem soils moreclosely than with annual crops (54, 106, 159).Furthermore, perennial plants restore functionin water infiltration and reduce compactionand, thus, increase rooting depth.

Plant species have greater effects on mi-crobes and plant-parasitic nematodes, trophiclevels with which they most intimately interact,than they do on predatory nematodes (158).Plants affect plant-parasitic nematodes at thespecies level (153) rather than at more coarselevels such as plant diversity (158) or plantfunctional group (154). However, functionalgroups of plants (i.e., legumes, forbs, grasses)have contrasting rooting patterns that createhabitats more favorable to some species ofnematodes than others. For example, mobileecto- and semi-endo-parasites are more com-mon under grasses, whereas sedentary ecto-and endo-parasites are more abundant underforbs where the soil tends to be fungal dom-inated (158). Communities of plant-parasiticnematodes can be complex within the rhizo-sphere of a single plant species. For example,the rhizosphere of marram grass (Ammophilaarenaria) in coastal dune systems provides habi-tat to a community of plant-parasitic nematodespecies that are controlled by factors ranging

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Trophic level:position in the foodchain determined bythe number ofenergy-transfer stepsto that level

Energy pathway:linkages betweenproducers andconsumers designatedby energy expressed asflux rates

Bottom-upcontrolled:dependence ofcommunity structureon factors, such asnutrient concentrationand prey

Top-downcontrolled: refers tosituation whereabundance, biomass,or diversity of lowertrophic levels dependson the effects ofconsumers fromhigher trophic levels;demonstrated by anincrease of thepopulation when thepressure of itspredators is decreased

from substrate resources, other organismsin the same position in the food chain, andpredators in higher trophic positions (122).

Soil Food Webs

The concepts of population and ecosystemecology integrate at the soil food web (13). Abasic soil food web has a similar structure tofood webs of other environments. Plants andorganic debris provide habitat for soil floraand fauna. In grassland, desert, and forestedecosystems, about 5% of net carbon flow entersthe above-ground grazing or consumer com-ponent, and the remainder enters the detritalfood web (24). Three basic energy pathwaysexist in soil: plant tissue, bacterial, and fungal(98). The plant tissue pathway includes primaryherbivores such as pathogenic nematodes andtheir consumers. These organisms decreaseprimary productivity of the plant by alteringuptake of water and nutrients and may createabnormalities in root morphology and/orphysiology. Energy and nutrients obtainedby plants eventually become incorporated indetritus that support the bacterial and fungalpathways. The bacterial or fungal pathwaysinclude saprophytic and pathogenic bacteriaor fungi and their respective nematode con-sumers (e.g., bacterivorous or fungivorousnematodes). The root, bacterial, and fungalpathways unite at levels higher in the foodchain, i.e., omnivores and predators. Secondaryand tertiary consumers graze on species inany of the trophic groups beneath them. Forexample, omnivorous nematodes feed on avariety of food sources, including algae, fungi,bacteria, small rotifers, enchytraeids, and smallnematodes (167). This grazing activity regu-lates energy and nutrient flows more than theirpopulation dynamics and biomass suggest.

In North America, short-grass prairie(Bouteloua gracilis), lodgepole pine (Pinuscontorta subsp. latifolia), and mountain meadow(Agropyron smithii) have similar food web struc-ture (76). They contain primary producers,consumers, and detritivores. The number andbiomass per volume of soil organisms decline

by orders of magnitude from bottom to toppositions in the food chain. Although structureis conserved across ecosystems, relative abun-dance of organisms within trophic or functionalgroups may vary by ecosystem type (117). InPoland, bacterivorous and plant-parasiticnematodes are the most abundant nematodesin agricultural soils, omnivorous nematodes aremore common in grasslands than agriculture,and fungivorous nematodes are relativelymore abundant in forest than agricultural soils(117, 159). In contrast, relative numbers ofnematodes in each functional group differ inSwedish soils. For example, ratios of organismsin fungal to bacterial pathways are greatest infertilized barley (Hordeum vulgare L.), followedin descending order by meadow fescue (Festucapratensis L.) and lucerne ley (Medicago sativaL.) (8).

A major question in soil ecology is whethersoil food webs are regulated by resources(bottom-up controlled) or by predators (top-down controlled). Nematodes hold a centralposition in food webs and impact ecologicalprocesses both directly and indirectly, suggest-ing that they play a critical role in ecosystemfunction (73). Detritus-based food webs arethought to be bottom-up controlled because oftheir characteristically large number of species,complex structure, abundance of omnivores andresource generalists, long food chains, paucityof top predators, and spatial heterogeneity(12). These are characteristics associated withdirect feeding interactions between links inthe food chain. Nematodes disperse microbesresiding on their body or in their gut, andslight to moderate grazing of nematodes onmicrobial populations is known to stimulatemicrobial growth (55). It is assumed that thistype of grazing preference maintains a bacterialpopulation in a youthful state and maintainsdecomposition activity. However, it has beensuggested that soil food webs are not exclu-sively bottom-up controlled but sometimesregulated by top-down mechanisms associatedwith indirect interactions (89). For example,predatory nematodes sometimes demonstratestronger relationships with the amount of



Communitystructure: list ofspecies and theirrelative abundances ina community

microbial food source than the abundance ofbacterivorous nematodes, which may servemerely as a conduit by which resources passfrom the bottom to top trophic levels (156).However, top-down regulation of microbial-and plant-feeding nematodes by predatorynematodes has been reported by others (169).These mixed observations support the theoreti-cal approach of de Ruiter et al. (34), who suggestcontrol is both bottom up and top down (12).

PHYSICAL HABITAT

Ecologists discuss habitat structure in terms ofaccessible resource distribution. In soils, habitatstructure is complex because of a combinationof physical constraints imposed by pore struc-ture, varying soil moisture, and resource distri-bution (plant roots and organic debris). Thus,natural selection is likely to act on consortiumsof microorganisms within this physical matrixrather than on individuals (27). Typically, soilecologists restrict considerations of pore or spa-tial structure to soil texture, i.e., grain size dis-tributions (40, 67). Although soils with sandytexture are less porous than finer soils, the vol-ume of pores large enough to be habitable fornematodes is greater in sandy soils than in finersoils. Fine soils provide more refuges for mi-crobes that are inaccessible to their nematodegrazers, thus diminishing the mineralization ofmicrobial biomass by grazing. For these rea-sons, mineralization of microbial populationscaused by nematode grazing is predicted to begreater in sandy than fine soils.

Aggregates as a Secondary Structure

In natural soils, soil particles are glued togetherby bacterial polysaccharides, interlaced byplant roots and fungal hyphae and otherorganic or mineral materials to form ag-gregates and provide a secondary structure.Therefore, formation and degradation ofaggregates is linked to plant and fungal growth,decomposition, and soil water dynamics (140).Aggregates are organized hierarchically withsmaller aggregates forming larger ones, cre-ating habitat for nematodes. Distribution of

nematode size is correlated with distributionof aggregate size (129). Different organismsmay be associated with pore size refugia atdifferent levels of aggregate organization. Forexample, bacterial density is greater insidethan outside aggregates. As a result, nematodegrazers that remain within aggregates may bemore efficient than those that forage in spacebetween aggregates. Under dry conditions,voids between aggregates may generate a net-work of isolated dry patches because generallywater drains more quickly from the largestpores. Thus, bacterivorous nematodes areconfined near their food source in aggregatesafter interaggregate spaces have drained (59,116). The close proximity of nematode grazersand microbial prey connect ecological and bio-geochemical processes, accelerating nutrientturnover and carbon mineralization (134). Forenclosures to form, aggregates need to remainmoist while becoming separated hydrologicallyfrom each other under unsaturated conditions.It has long been observed that aggregationlowers the water potential at which plants reachtheir permanent wilting point. Likewise, largepopulations of Aporcelaimellus nematodes havebeen observed at water potentials of 50 kPawhere only pores ≤10 μm remain water-filled(116). Understanding the impacts of hierarchi-cal soil structure is an important considerationfor future investigations both in terms ofcommunity structure and function. Althoughaggregate structure modifies the relationshipbetween soil fauna and texture, only a fewecologists and nematologists have consideredaggregates as habitat for soil nematodes (165).

Foraging Patterns

Structure of physical habitat not only affectsresource distribution, but also selects for theforaging and predation strategies of its in-habitants. Soil structure may affect foragingefficiency of nematodes directly by forcingthem to follow paths longer and more tortu-ous than if no spatial partitions existed (1) orby confining them to isolated water-filled re-gions within aggregates. Within confined areas,

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Correlatedmovement: randompattern of movementwhere absolute moveangles are correlatedrelative to a fixedcoordinate system

Age structure:distribution ofindividuals in variousage classes within apopulation

compensatory growth of bacteria is stimulatedby nematode feeding, thereby providing nema-todes with more food. In homogenous environ-ments, nematodes exhibit deliberate, correlatedmovement (66), which creates patterns that ex-plore larger areas than simple random walks.When an attractant is present, nematodes relyon chemotaxis, making foraging more efficient(119). When structure is present, foraging be-comes more of an avoidance strategy, allow-ing nematodes to escape structural traps suchas dead-end pores (1). Bacterivorous nematodesappear to forage continuously on bacteria (171).However, individuals within populations differin movement, with some moving fast and mak-ing large loops, whereas others move slowlyand fluctuate between backward and forwardmovement (66). Given that entomopathogenicnematodes have contrasting interspecific for-aging strategies within a trophic group (90),it is expected that free-living nematodes alsovary in spectrum from generalist to specialistforaging strategies among species. Further, ca-sual observations from life-history studies sug-gest that populations of mixed age structure( juvenile versus adult) may also exist in bac-terivorous nematodes that contrast in foragingbehavior (D.A. Neher & T.R. Weicht, unpub-lished data).

Niche Partitioning

The field of soil ecology encounters manycontemporary challenges of ecological the-ory, such as resolving the apparent conflictbetween competitive exclusion, observedbiodiversity, and functional redundancy withina heterogeneous environment (4). Individualtaxa may have multiple functions, and severaltaxa appear to have similar functions (139).Functionally redundant species may representa form of biological insurance against speciesloss by natural population cycles or disturbance(101). However, the impression of functionalredundancy may be exacerbated by the scarceknowledge of basic biology and ecology offree-living nematodes, anonymity of most soilorganisms, trophic position, and heterogenous

distribution of resources (102). Proponentsof functional redundancy have been criticizedfor conclusions based on structurally simplemicrocosm experiments that contain far fewerspecies than field communities (5). In addition,redundancy within a trophic group fails toexplain why contrasting species of bacteri-vores contribute differentially to nitrogenmineralization (49, 124) or coexist in riparianareas (43). Although species may appear tobe functionally redundant, taxa performingthe same function are often isolated spatially,temporally, or by microhabitat preference (9).

Ecologists have long been perplexed by thequestion of how so many species can coexistwhile using the same resource (75). This para-dox can be resolved by assuming there are asmany different resources as there are differ-ent species (91). Competing species can avoidcompetitive exclusion when individuals occupyresource patches that diverge in their physi-cal, biological, and chemical nature. Moreover,distinct physiological and environmental re-quirements drive species of the same functionalgroup to play contrasting roles in soil ecosystemprocesses. For example, three genera of bac-terivorous nematodes respond to different soiltypes and moisture status in the same way, sug-gesting the diversity within nematode assem-blages contributes to resilience in biologicallymediated soil processes (168). As poikilotherms,nematode species grow optimally over a limitedtemperature range. Therefore, communitiesexhibit a seasonal dynamic where the dominantspecies differs through time (50). Not only doestemperature vary by season, but so does quan-tity and quality of plant litter as a food resource.

Soil pore size distribution may provideniche separation with each pore size categoryrepresenting a niche for soil fauna of similardiameter. However, viewing pore size as asole niche separator is simplistic. Other nichedimensions include diet, foraging strategy, andbody size (53). Nematodes occupy existingpore spaces and respond to soil water dynamicsas air-filled and water-filled pore size distribu-tions oscillate. Soil moisture variation inhibitsor encourages consumption by affecting



habitat overlap between consumers and pro-ducers and by creating a dynamic partitioningof habitat within and among aggregates.Temperature and moisture affect rates ofassimilation, respiration, and reproductiondifferently for each nematode species (48,49, 99). Nematodes are sensitive to extremetemperatures, especially in moist soils wherethey are active (28). In hot, dry soils, nematodescan survive anhydrobiotically near roots or ininteraggregate spaces. Species within a trophicgroup differ in sensitivity to temperature,which may reduce interspecific competition(2). Combinations of nematodes of differentlife strategies may lead to more thorough ex-ploitation of a food source and, consequently,higher nitrogen mineralization.

Developmental stages of nematodes differ inrelative survival. Infectivity of plants by nema-todes can differ with life stage and nematodeshave survival structures that operate at multiplelife stages. For example, eggs are protected bythick-walled tissue or within cysts. Third-stagejuveniles may convert to a dauer stage eitheras a survival or phoretic dispersal mechanism.Juvenile and adult stages may transition intoanhydrobiosis with drought conditions. Thesephysiological adaptations allow nematodes toinvade and tolerate habitats in which few otheranimals can survive, and to avoid interspecificcompetition and many environmental selectionpressures. Although nematodes have adaptivemechanisms to survive extremities of climate,their activity is stimulated by the return of moremoderate conditions. For example, communi-ties of nematodes are revived within minutesafter rain in desert soils (28) or shift quickly be-tween active and inactive states in response tosmall, diurnal changes of temperature or rela-tive humidity in Antarctic soils (146).

ECOSYSTEM FUNCTION

Soil ecologists recognize that the structureof detrital food webs is reflective of ecosys-tem function, but few studies have explicitlyexplored these connections (12). Ecosystemfunctions include primary productivity (yield

or plant growth), decomposition and nutrientcycling, disease suppression, and biologicalcontrol. Mechanisms of these functions canbe abiotic or biotic. For the management anddevelopment of sustainable ecosystems, it isprobably most important to understand therelationships between energy and associatednutrients among functional groups.

Primary Productivity

Plant-parasitic nematodes decrease primaryproductivity of their hosts by consumingthe cytoplasm of plant cells, triggering planthormone responses that change source-sinkrelationships, and physically destroying roots.While feeding, the nematode may exist outsideor inside the root and either remain sedentaryor migrate through plant tissue. Negativeeffects of plant-parasitic nematodes are betterdocumented than positive effects. However,an example of the latter is that low levels ofbelow-ground herbivory of clover-by-clovercyst nematodes (Heterodera trifolii) increasesroot growth in grassland mixtures of whiteclover and Lolium perenne (7). Other studiesshow no net effect of total abundance ofnematodes on tallgrass prairie (136) but doshow a positive effect for short-grass prairie(77) or mid-successional grasslands (29).

Decomposition

Within the detrital community, bacterivorousnematodes play significant roles in regulatingdecomposer microflora composition (36), litterdecay rates, and element cycles (6, 52). Ratesof decomposition are affected by the number oftrophic levels and their interactions (13, 138).Decomposition rates are sensitive to physicaldisturbances such as cultivation (110). For ex-ample, decomposition rates are 1.4 to 1.9 timesfaster in conventional than no-till soils withresidues remaining on the surface (8). Fungiand fungivorous nematodes are more likely toregulate decomposition of surface residues inno-till soils, whereas bacteria and bacterivorousnematodes regulate decay rates in incorporated

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residues in conventional-till soils. The relativedominance of fungi and fungivorous nematodesin early stages of decay of surface residues canbe explained by the initially high ratio of ligninto nitrogen. Bacteria and bacterivorous nema-todes move in as secondary colonizers after de-cay is initiated.

Nutrient Cycling

Detrital pathways are responsible for the great-est proportion of nutrient mineralization in ter-restrial ecosystems. Carbon and nutrients areinextricably linked in all food webs (61). Nema-todes affect nitrogen availability both directlyand indirectly (77). Directly, nematodes excreteammonium as a byproduct because their preygenerally has a lower ratio of carbon to nitrogenthan nematodes need. Indirectly, they liber-ate nitrogen immobilized by microbes throughmetabolism and excretion and disperal of mi-crobes to more suitable substrates. Bacterivo-rous and predatory nematodes are estimated tocontribute (directly and indirectly) about 8%to 19% of nitrogen mineralization in conven-tional and integrated farming systems, respec-tively (8). Net nitrogen mineralization is tem-pered by immobilization by fungi (8) in Swedishforest soils and by bacterivorous nematodes inlow fertility deserts soils in Utah (28).

Disease Suppression/BiologicalControl

Although some nematodes are the causal agentof disease and, thus, the target of biocontrol,others are predators that can control a diseasecaused by a bacteria or fungus (169). Mecha-nisms suggested to control plant-parasitic ne-matodes include competition, arbuscular my-chorrhizal fungi, endophytic fungi, and plantresistance (151). Mechanisms originating withthe plant are called bottom-up interactions be-cause they are driven by limitation of resourceavailability. Coastal dune systems exemplify allof these mechanisms (122). The root zone ofmarram grass (Ammophila arenaria) containsa mixture of plant-parasitic nematode species

that each respond in a different manner. Forexample, the cyst nematode Heterodera are-naria is controlled by host nutrients and soilmicrobes, whereas the lesion nematode Praty-lenchus penetrans is suppressed by prior col-onization of roots by arbuscular mycorrhizalfungi (32, 131). Fungi can also alter competi-tion between species of plant-parasitic nema-todes within a single rhizosphere (71).

Plant-parasitic nematodes can also be con-trolled by predators or parasitic soil organ-isms (85) such as soil microbes, predator ne-matodes, microarthropods, and tardigrades.Bacterial species of Pasteuria and the nema-tode trapping fungus Hirsutella rhossiliensis par-asitize root-knot and cyst nematodes (81, 127).Diplogasterid nematode predators (e.g., Odon-topharynx longicaudata) are well suited for bio-control of nematodes, because they are easyto culture and have short life cycles, prey-specificity, and resistance to adverse conditions(86). Mononchidae (e.g., M. fortidens, M. long-icaudatus, M. gaugleri) have been consideredto be unsuccessful for biocontrol because oftheir scarcity, long life cycle, and sensitivityto environmental disturbance. In infertile nat-ural areas, abundances of Discolaimus, Tripyla,and Prionchulus nematodes have been ob-served to suppress root-knot nematodes (133).Physical or chemical properties of soil that in-fluence disease suppression of plant-parasiticnematodes include pore structure, pore con-nectivity, water-air balance, organic matter, andpH (57). Subsistence agriculture has relied ontraditional knowledge to favor beneficial organ-isms by cultivation methods and appropriate useof soil amendments, sanitation, crop rotation,fallow, adjusting planting time, including an-tagonistic and trap crops, artificial and naturalflooding, and burning stubble (18). These prac-tices were not necessarily based on scientificknowledge but were empirically determineddue to the prohibitive cost of nematicides.

ECOLOGICAL THEORY

Ecological theory developed from the studyof above-ground and aquatic systems has been



Stability domain:ability to withstandperturbations withoutlarge changes incomposition

Diversity index:measure of the varietyof species in acommunity that takesinto account therelative abundance ofeach species

applied to soil communities but incompletelytested. Soil communities are unique becauseomnivory is more prevalent than in other com-munities. Above-ground predators are usuallylarger than their prey, whereas this is not truein the soil, as soil pores constrict size differ-ences between predator and prey. Omnivoryis an advantage in a heterogenous distribu-tion of uncertain food items (37). Perhaps, theprevelance of omnivory in soil communitiesnegates the existance or role of keystone taxa(123) because it produces complex interactions,making it impossible to make broad trophic-level generalizations. Further, omnivory maybe prevalent because soil physical partition-ing disrupts trophic interactions. Moore et al.(97) demonstrated that soil food webs canbe stable in the presence of omnivory be-cause the resource base is greater than thatconsumed.

Even though soil habitats are unique fortheir spatial constraints, similarities with otherhabitat types should not be ignored. Onepossible similarity is that the optimal foragingstrategy among bacterivorous nematodes insoil is synonomous with the “green world”hypothesis (“The world is green because it isprickly and tastes bad”) proposed by Hairstonet al. (65). Generalist herbivores seek a varieddiet to tolerate or dilute exposure to plantdefense chemicals, whereas specialists havecoevolved tolerance to these chemicals. Likeplants, microbes produce multitudes of defensecompounds that could be detrimental to theirgrazers. Bacterivorous nematodes are likelygeneralists with varied diets to reduce theimpact of microbial toxins. Some fungivoresare specialists that exhibit contrasting growthrates on different fungal species (118).

Ecologists debate whether measures of bio-diversity are directly proportional to ecosystemstability (93). One explanation is that soils arethe largest reservoir of biodiversity. Therefore,soil function has been demonstrated to be re-silient to disturbance. Nematode communitiesoffer a model system to evaluate ecologicaltheory in soils. Ecological succession of nema-tode communities have been studied but many

questions remain relating to where, how, andwhy particular species are present, what theyeat, and the type of interaction they have withother species in the food web.

Biodiversity and Ecosystem Stability

One can hypothesize that in a stable systemeach microhabitat is occupied by organisms thatwere first present and/or best able to colonizethe niche and become established, and nicheoverlap is relatively small. Understanding therelationship of biodiversity to ecosystem func-tion and stability is of importance to scientistsinvolved in environmental monitoring, eco-logical restoration, and sustainable agriculture.Stability is defined as the ability to withstandor to recover from a disturbance. This defi-nition is sometimes used synonymously withthat of resilience or resistance. Resilience isthe ecological memory or capacity of a systemto absorb disturbances, reorganize, and main-tain adaptive capacity before shifting to anotherstability domain (63, 120). A sufficient reser-voir of community members remain so thata system can be recolonized and return to itsoriginal equilibriuim, reestablishing ecosystemfunction. A combination of two scenarios mayfacilite ecosystem resilance: (a) local, internal,or within-patch organisms that survived the dis-turbance and (b) external sources of organismsthat can disperse and recolonize a system.

Many grass-roots conservation and restora-tion groups promote greater diversity as ameans to achieving ecosystem stability (141)because species richness may preserve function(72). However, many ecologists claim that bio-diversity itself (number of species or speciesrichness) is not a good predictor of stability, (79,93) and controversy remains. Gross et al. (62)suggest food web stability is enhanced whenspecies at intermediate trophic levels are fedupon by multiple predator species.

Index values of species richness simply rep-resent the number of taxa, not the identity orecological diversity of species. Consequently,a community of invasive taxa could have thesame diversity index as a community of native

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taxa. A diversity index is simply a mathematicalvalue that represents an inseparable integrationof species numbers and equality or evennessof abundance among species (80). Nematodediversity can be assessed at the species, genus,or trophic level (111). At the trophic level, it isa measure of food chain length and food webcomplexity. A trophic diversity index assumesthat greater diversity of trophic groups insoil food webs, and longer food chains reflectimproved ecosystem function (95). Generally,diversity assessed at the genus or trophic reso-lution of soil nematodes is greater in perennialand natural systems than annual croppingsystems, with or without cultivation (54). Incontrast, Neher (104) found little differencein trophic diversity (food web complexity) be-tween conventional and organic farms, neitherof which was fumigated with general biocides.Reducing the frequency of cultivation (68)and including perennial crops in agriculturalsystems (54, 106, 159) are two ways to increasetrophic diversity in arable soils.

ECOLOGICAL SUCCESSION

The successional status of a soil community mayreflect the history of disturbance. Succession incropped agricultural fields after cultivation andclearing of native vegetation shifts a commu-nity to an earlier stage of succession that favorsa relative abundance of opportunistic species,such as bacteria and their predators, who colo-nize the soil. The communities are dominatedby organisms with short generation times, smallbody size, rapid dispersal, and generalist feed-ing habits such as bacteria and bacterivorous ne-matodes (10). Subsequently, relative abundanceof fungi and fungivorous nematodes increasein the area. Secondary and tertiary consumersor predators establish later. Macrofaunal diver-sity is hypothesized to be greatest at intermedi-ate stages of succession where early- and late-staged taxa coexist (69, 121). This intermediatedisturbance hypothesis could explain why somegroups of organisms are more abundant in no-till (i.e., intermediate disturbance) than eitherconventionally tilled (i.e., extreme disturbance)

or old-field (i.e., no disturbance) systems (155).If disturbance is common or harsh, only a fewtaxa that are resistant to disruption will per-sist (121). If disturbance is mild or rare, soilcommunities will approach equilibrium and bedominated by a few taxa that can outcompete allother taxa. However, attainment of steady-stateequilibrium in agricultural or natural ecosys-tems is rare. Succession of nematode commu-nities has also been well described for a pineforest (33), during formation of compost (142),and after application of compost (42).

Succession can be interrupted at variousstages by disturbances. Two major types of dis-turbance in agricultural systems, physical andchemical, are often intertwined in managedecosystems (51). Physical disturbance includescultivation and compaction by repeated passesof heavy machinery. Such cultivation shifts agri-cultural soils to an early stage of succession (106,155). Alternatively, reduced tillage leaves mostof the previous crop residue on the soil sur-face, and this results in changes in the physicaland chemical properties of the soil (68). Surfaceresidues retain moisture, dampen temperaturefluctuations, and provide a continuous substratethat promotes fungal growth. Chemical distur-bance includes amendments for fertility and ad-dition of organic matter and/or pesticides, allof which are substrates for bacteria. Therefore,these amendments favor the bacterial channel(165) and provide a general enrichment phe-nomenon (103). High levels of fertility and nat-urally saline soils generate osmotic stress thatis detrimental to the survival of many nema-tode species (145). A combination of cultiva-tion and fertilizer reduce the flow through thefungal channel and decouple the regulation ofnitrogen mineralization and decomposition byorganisms higher in the food chain comparedto grassland ecosystems (17, 96).

Disturbance can also be characterized byintensity and duration, expressed as acute orchronic, pulse or press (11, 152). Chronic orpress disturbance can lead to gradual species ex-tinction and eventually decreases resiliency ofan ecosystem to disturbance or disruption (79,120). Monoculture agriculture or long-term



Maturity index:nematode communityindicator of ecologicalsuccession or measureof disturbance; largervalues represent alate-successional stagecommunity

exposures to soil polluted with heavy metals aretypes of chronic disturbance.

Measures of ecological succession of ne-matode communities include the fungivore tobacterivore ratio, as well as maturity, channel,and structure indices (15, 47). The fungivoreto bacterivore ratio reflects the successionalstage of the decomposer community. Thenematode maturity index (15) is based onrelative sensitivity of various taxa to stress ordisruption of the successional pattern. Origi-nally, the maturity index was based separatelyon community composition of free-living andplant-parasitic nematodes (15, 54), but thereis debate on whether that is necessary (107,164). Recommendations for environmentalmonitoring on large geographic scales are tocalibrate these nematode community indicesby ecoregion (112) and ecosystem type (117).Indices that describe associations within nema-tode communities, such as the maturity index,are less variable than measures of abundanceof a single nematode taxonomic or functionalgroup, and are more reliable statistically asmeasures of ecosystem condition (107, 113).

BIOGEOGRAPHY

Since Charles Darwin, ecologists have beenintrigued with how and why community assem-blages vary among habitat patches, geographicregions, or islands. Explanations have rangedfrom latitudinal differences in climate (128),habitat heterogeneity, and niche partitioning(75), to island biogeography theory (IBT).IBT predicts that isolation by island or habitatarea drives species richness and suggests apositive association between species richnessand land area because large areas attract moreimmigrants, hold larger populations, anddecrease the risk of stochastic extinction (91).Geographic isolation also accounts for speciesisolation and evolution and reduces potentialcolonists. IBT was developed for plant andvertebrate species and has yet to be tested thor-oughly for invertebrate taxa, especially thoseresiding in soil (82). Only recently are nema-tode community assemblages being examined

from an IBT perspective. For example, nema-todes have been studied for island systems in theAntarctic (92) and Hawaii (14), for lake islandsin the boreal forests of northern Sweden (82),and for epiphytes as islands of different sizesand on different tree species in New Zealandrainforests (158). To date, ecosystem attributes(e.g., decomposition or respiration rate, nitro-gen or phosphorus loss), plant associates, inter-actions of temperature and moisture regimes,and niche partitioning appear to be better pre-dictors of species richness than IBT (82, 158).

Latitudes differ in patterns of tempera-ture and precipitation, resulting in contrast-ing biomes. The latitudinal gradient hypothesispredicts that biodiversity of biota will be greaterin tropics than temperate zones, although ne-matodes may be an exception. Procter (128) at-tributes the relatively low tropical nematodebiodiversity to an inability to compete withmore specialized organisms in the tropics, andsuggests that nematodes are more adaptable andtolerate climate-induced stress typical of higherlatitudes. However, this interpretation of lati-tudinal gradients was based on soil samples thatare relatively thin in tropical systems. When lit-ter and understory habitats are sampled in addi-tion to mineral soil, nematode species richnessin a Costa Rican tropical rainforest is compara-ble or exceeds that of temperate latitudes (126).Detritus and root substrates are more abundantabove than below ground in tropical rainforests.

Colonization of new patches depends onthe ability to move between patches, perme-ability of corridors, distance between patches,and accessibility of patches. These parametersare structural in nature. Nematodes can be dis-persed to new habitats by wind, water, andbiotic vectors. Under climax conditions, ne-matodes are constantly supplied, but the lackof suitable niches generally prevents popula-tion establishment. If soil aggregates are re-sources, interaggregate spaces define the mini-mal distance that organisms need to travel fromone patch to the next. Accessibility to patchesdepends on the pore sizes leading into an ag-gregate. Pore sizes at the surface of an ag-gregate may determine the vulnerability of

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organisms within the aggregate to predationfrom the outside. Colonization sequence andrecruitment in soil patches may depend on soilmoisture because it determines patch connec-tivity and corridor permeability for animals ofdifferent body sizes and locomotion modes.

Many soil-dwelling micro- and mesofaunacan reproduce parthenogenically. Partheno-genesis is an r-selected trait, allowing coloniza-tion in the absence of mates and usually resultsin faster population growth rates, potentiallyaccelerating energy and matter fluxes throughthe food web.

Designing Agricultural Systems withCommunity Approaches

Modern agricultural methods have reliedheavily on nonrenewable natural resources,especially soil and ancient groundwater (44).Petroleum products for fuel, pest management,and fertility have replaced or substitutednatural and seasonal patterns of ecologicalprocesses with synthetic materials. Designingagricultural systems that more closely mimicnatural ecosystems will rely on a greaterworking knowledge of ecology and evolution.Natural ecosystems, whose components arethe results of natural selection, are sustainable;most are productive, responsive to pests, andretentive of nutrients (44). Agricultural soilswould more closely resemble soils of naturalecosystems if management practices reduced oreliminated cultivation, including use of heavymachinery and general biocides, and incorpo-rated perennial crops and organic material (41,103). Uncultivated soil typically has greateraggregate structure, higher organic matter, andmore tilth than cultivated soil (58). Generally,research shows that physical disturbance ismore disruptive than chemical disturbance(103, 105), although general biocides kill manynontarget predators of the pest or pathogentarget (42, 108). Perennial crops have largerroot systems than annuals and, thus, providelarger rhizosphere habitats to support complexsoil food webs and help to reduce soil erosionbecause of a longer growing season, fewer in-puts of pesticides and fertilizers, fewer passes of

farm machinery, and greater carbon sequestra-tion (58). Organic amendments have numerousbenefits, including improved soil tilth, reten-tion of water and nutrients, and providing asubstrate to support beneficial organisms thatallow natural competitive, antagonistic, andmutualistic relationships to occur (85). Organicmatter includes microbes as well as bacterivo-rous and fungivorous nematodes that enhanceecosystem processes such as decomposition,nutrient mineralization, and disease suppres-sion. Although it is difficult to separate their in-dividual effects, concurrent addition of organicmatter and elimination of general biocideshave the benefit of allowing omnivores andpredaceous species to increase in prevalence,which promotes natural disease suppression(147).

Essential Research

Ecological research on nematodes is morethan simple observation, enumeration, andidentification (45, 130). Given their central rolein the soil food web and linkage to ecologicalprocesses, nematodes can be a tool for testingecological hypotheses and understandingbiological mechanisms in soil. A limitednumber of ecological hypotheses have beentested using soil nematodes. However, manyother hypotheses that are not yet tested havepotential applications for contributing to moresustainable agricultural systems, includingimproved strategies for biological controland disease suppression, and environmentalmonitoring. These studies may ultimately leadto development of improved soil ecologicaltheory to understand the impacts that soilfauna have on system processes.

Synchronizing nutrient release and avail-ability relative to plant needs is critical forimproving nutrient use efficiency and lim-iting pollution by excess nutrients. Nema-tode abundance and environmental propertiesare often measured simultaneously for prac-tical reasons. However, time lags exist be-tween relative abundance of nematodes andsubsequent availability of nitrogen (170; D.A.Neher & M.E. Barbercheck, unpublished data).



The need for better resolution of these timelags has practical consequences for designingsampling schedules to test ecological hypothe-ses related to herbivore-host, pathogen-host,and grazer-food resource questions. Failure toconsider time lags may lead to potentially erro-neous interpretation of these relationships.

We need to understand ecological theoryto better manage our soils. Within the past20 years, useful tools have emerged in molec-ular biology (132), stable isotopes (20), com-plex systems modeling, and in situ techniques toquantify pore networks in soil. These tools offersome exciting possibilities to identify ecologicalmechanisms related to niche partitioning (169),optimal foraging (30), and biogeochemicalcycling (156, 161).

Monitoring and Restoration

Currently, a major limitation in implementa-tion of maturity indices is the lack of publicand commercial laboratories with the knowl-edge and personnel to handle large numbersof samples for identification of free-livingnematodes (105). Identification of sentineltaxa that predictably respond to specificdisturbance types and respond quantitativelyto intensity of disturbance will allow develop-ment of molecular-based tool kits that can beused by nonspecialists. For example, Neher& Sturzenbaum (114) developed a generalbiomarker approach that quantifies DNAdamage of nematode species that are relativelysensitive to toxic chemicals and/or unableto repair their DNA to its original sequence(potentially creating lethal mutations) whenexposed to relatively high doses of polycyclicaromatic hydrocarbons, but are unresponsivewhen exposed to a heavy metal. Briefly, thisapproach performs PCR on relatively long(12K bp) fragments of DNA followed byquantitative PCR. Long sequences are neededto increase the probability that they containmisreads and will not amplify properly. Unfor-tunately, primers developed for Caenorhabditiselegans do not work for other bacterivorousnematodes, including members of the families

Cephalobidae and Panagrolaimidae, and thegenus Plectus (D.A. Neher, unpublished data).Sequence determination of extended lengths ofDNA is needed for the free-living nematodesrecognized as sentinel taxa. To date, sequenceinformation has been biased toward plant-parasitic nematodes of economic concern (125).Before discontinuing traditional morpholog-ical identification of sentinal taxa, it will benecessary to link extensive morphological fea-tures to diagnostic DNA sequences. Sequenceknowledge will be especially useful for taxa thatare morphologically similar and/or for identifi-cation of juveniles, which have fewer diagnosticfeatures. Such molecular operational taxonomicunits (MOTUs) have enormous potential tobecome useful for biodiversity surveys (126).

Indicator taxa must correlate or predictecosystem function to be of value for imple-mentation at regional or national scales. Link-age of taxa to ecosystem function is necessary toconvince other biologists and monitoring pro-grams of the utility of nematode communitiesas indicators. Nematologists are only begin-ning to identify sentinel taxa (39, 46, 51, 143)that represent a subset of nematode communi-ties. Identification of the most appropriate taxawill require knowledge of species assemblagepatterns under different scenarios of manage-ment practices, often representing a compli-cated mixture of abiotic and biotic factors (5,51). Newer computational techniques such asArtificial Neural Networks (88) and null mod-els (60) in conjunction with current multivariatestatistical techniques may help to link individualtaxa with habitat conditions. Subsequent stud-ies are needed to verify the sentinel status ofspecific taxa and to determine the geographicor ecological range of their utility. These ex-periments should be conducted to quantifyimpacts of multiple and interacting manage-ment practices on biodiversity, nutrient cycling,pest populations and plant productivity.

Microbial complexity also increases posi-tively with chemical complexity of the sub-strates (100). If optimal foraging of bacteriv-orous and fungivorous nematodes occurs, thenone would expect that at least a portion of the

384 Neher


Donor controlled:extreme case ofbottom-up controlwhere donor (prey)controls the density ofthe recipient(predator)

Trophic structure:organization of thecommunity based onfeeding relationshipsof populations

food web is donor controlled because diversityof lower trophic nematodes would increase withcomplexity of organic substrates and the mi-crobial decomposer community. This hypoth-esis assumes many microbial species exude toxiccompounds for defense. Nematodes must for-age on a varied diet to reduce toxicity and in-crease nutrition.

Spatially explicit concepts of population dy-namics based on the interaction between in-dividuals are a new approach to look at com-plex systems. In soils, spatially explicit modelshave to function within a spatially partitionedand diverse environment. Quantitative modelsof age-structured populations that are scale-appropriate, three-dimensional estimations ofhierarchical soil structure would improve pre-dictions of the impact of soil nematodes ontheir contribution (direct or indirect) to eco-logical processes such as nitrogen mineraliza-tion. These models require more detailed lifehistory experiments that quantify feeding, res-piration, and biomass (115), as well as reproduc-tion dynamics at the level of genus and speciesand population age structure. Spatially explicitmodels will enhance existing soil models thatrelate trophic structure to ecosystem functionbut fail to treat soil heterogeneity at scales rele-vant to soil microbes (2–4 μm) and microfauna(5–100 μm) and thus misrepresent the contri-bution of different taxa. Because spatially ex-plicit models are required on the pore-scale ofsoils, there are current limitations in existing in-strumentation, media resolution, and computercapacity. Emerging models will be required toincorporate efficient computational techniquesto adjust observation from life-history studieswith observation at the field and microcosmscales.

Relatively little is known about nematodecommunity assemblages and species in naturalterrestrial ecosystems. These natural systemscan be valuable as reference points for environ-mental monitoring or ecological restorationefforts (117). They can also be study sitesto learn biological mechanisms for diseasesuppression and host-pathogen relationships.Resulting models are useful to generate and test

hypotheses of the attenuation of interactivestrength in soil food webs of controlled andfield settings.

Nematodes are important components ofthe soil community with substantial effects onsoil ecosystem processes and plant communitystructure (6, 31, 130, 150). Soil nematodes af-fect the composition of natural vegetation andmay cause dramatic shifts in vegetation dynam-ics through time (29). Herbivory and diseasecaused by plant-parasitic nematodes rarely killthe host plant but can reduce competitivenessof affected plants. Changes in competitive re-lationships among plant species can influencedirection and rate of succession. Effects ofabove-ground herbivory on plant competi-tion are relatively well studied, but the role ofbelow-ground herbivory is gaining recognition,especially in its role as a constraint to net pri-mary productivity in grassland systems whereplant-parasitic nematodes are numericallyabundant as root herbivores (78). Furthermore,selective grazing by plant-parasitic nematodescan affect competition between crop and weedspecies (22), establishment of clover in rye grass(26), and establishment of dune ecosystems(149). Further knowledge of these types ofbiotic interactions in soil has applications in therestoration and conservation of plant speciesdiversity.

Plant-parasitic nematodes and plant hostsin natural ecosystems have coevolved longerthan crop-nematode systems (19). Under-standing the mechanisms of the widespreadresistance and tolerance of wild plants couldbe useful to improving crop protection againstplant-parasitic nematodes (94, 148).

Finally, facilitative and inhibitory interac-tions between plants and nematodes requirefurther study to better understand below-ground plant defense (162). Plant exudatesare not always beneficial for plant-parasites.For example, root exudates of Leucanthemumvulgare, Ranunculus acris and clover (Trifoliumpretense) decrease populations of plant-parasiticnematodes in the rhizosphere (154). Some plantspecies contain and exude nematicidal com-pounds (23) and harbor nematode-suppressive



microbes in their rhizosphere (87). For exam-ple, Plantago is a nematode suppressing plantgenus (30). The mechanism is not clear, butgreater concentrations of glucose and fumaricacid occurred in root exudates of Plantago (162)

and barley (Hordeum vulgare) in the presence ofPratylenchus penetrans and Meloidogyne incognita,respectively (64). These effects were isolatedfrom those of other rhizosphere microbes in acontrolled experiment.

SUMMARY POINTS

1. Historically, nematology primarily addressed research questions related to disease man-agement by general biocides. Contemporary concerns about environmental degradationand global climate change provide incentives to revisit nematodes as pivotal ecologicalplayers in soil communities of agricultural and natural ecosystems.

2. Ecology is a branch of biology and contributes to our understanding of evolution, andmay focus on one or more scales, such as population, community, or ecosystem.

3. Nematodes are aquatic organisms that depend on thin water films to live and move withinexisting pathways of soil pores of 25–100 μm diameter.

4. Soils provide a complex hierarchical scaling of structure that includes pore distributionand aggregates. Habitable pore space oscillates in response to soil water dynamics. Fewnematologists or ecologists include physical constraints of soil habitat in experiments ormodels.

5. Given their central role in the soil food web and linkage to ecological processes, ne-matodes can be a tool for testing ecological hypotheses and understanding biologicalmechanisms in soil.

6. Ecological succession is one of the most tested community ecology concepts, and avariety of indices have been proposed for purposes of environmental monitoring. Incontrast, theories of biogeography, colonization, optimal foraging, and niche partitioningare poorly understood.

7. Ecological hypotheses related to strategies of coexistence of species sharing the sameresource have potential uses for more effective biological control and use of organicamendments to foster disease suppression.

8. Indicator taxa must correlate or predict ecosystem function to be valued for implementa-tion on regional or national scales. It is the linkage to ecosystem function that is necessaryto convince other biologists and programs of the utility of nematode communities asindicators.

FUTURE ISSUES

1. Release and availability of nutrient amendments synchronized to the timing of plantneeds would improve nutrient use efficiency and limit pollution of excess nutrients.

2. Biological control and use of organic amendments to foster disease suppression can bemade more effective by applying ecological concepts related to nematode strategies ofcoexistence of nematode species sharing the same resource.

386 Neher


3. Tools are needed to explicitly identify dietary preferences to allow for a greater under-standing of nematode ecology at a species or genus level.

4. Sentinel nematode taxa that predictably respond to specific disturbance types need tobe identified and verified to develop relatively simple molecular-based tool kits fornonspecialists.

5. Interpretation of nematodes as biological indicators of soil depends on quantifiable link-ages between indicator taxa and ecosystem function.

6. Quantitative models of age-structured populations that are scale-appropriate, three-dimensional estimations of hierarchical soil structure would improve predictions of theimpact of soil nematodes and their contribution to ecological processes.

7. Discovering community assembly patterns of soil nematodes under different scenarios ofmanagement practices will provide a reference for interpretation of nematode indicatorsused for environmental monitoring, conservation, and restoration.

DISCLOSURE STATEMENT

The author is not aware of any affiliations, memberships, funding, or financial holdings that mightbe perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

The author thanks Thomas R. Weicht for a critical and constructive review of an earlier draft.

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