Earthworms (Annelida:Oligochaeta) of theColumbia River BasinAssessment AreaSam James

United StatesDepartment ofAgriculture

Forest ServicePacific NorthwestResearch Station

United StatesDepartment of theInterior

Bureau of LandManagement

General Technical ReportPNW-GTR-491June 2000

Author

Sam James is an Associate Professor, Department of Life Sciences, Maharishi University ofManagement, Fairfield, IA 52557-1056.

Earthworms (Annelida: Oligochaeta) of theColumbia River Basin Assessment Area

Sam James

Interior Columbia Basin Ecosystem ManagementProject: Scientific Assessment

Thomas M. Quigley, Editor

U.S. Department of AgricultureForest ServicePacific Northwest Research StationPortland, OregonGeneral Technical Report PNW-GTR-491June 2000

PrefaceThe Interior Columbia Basin Ecosystem Management Project was initiated by the USDA ForestService and the USDI Bureau of Land Management to respond to several critical issues including,but not limited to, forest and rangeland health, anadromous fish concerns, terrestrial species viabilityconcerns, and the recent decline in traditional commodity flows. The charter given to the project wasto develop a scientifically sound, ecosystem-based strategy for managing the lands of the interiorColumbia River basin administered by the USDA Forest Service and the USDI Bureau of LandManagement. The Science Integration Team was organized to develop a framework for ecosystemmanagement, an assessment of the socioeconomic biophysical systems in the basin, and an evalua-tion of alternative management strategies. This paper is one in a series of papers developed as back-ground material for the framework, assessment, or evaluation of alternatives. It provides more detailthan was possible to disclose directly in the primary documents.

The Science Integration Team, although organized functionally, worked hard at integrating theapproaches, analyses, and conclusions. It is the collective effort of team members that providesdepth and understanding to the work of the project. The Science Integration Team leadership includeddeputy team leaders Russel Graham and Sylvia Arbelbide; landscape ecology—Wendel Hann, PaulHessburg, and Mark Jensen; aquatic—Jim Sedell, Kris Lee, Danny Lee, Jack Williams, Lynn Decker;economics—Richard Haynes, Amy Horne, and Nick Reyna; social science—Jim Burchfield, SteveMcCool, and Jon Bumstead; terrestrial—Bruce Marcot, Kurt Nelson, John Lehmkuhl, RichardHolthausen, and Randy Hickenbottom; spatial analysis—Becky Gravenmier, John Steffenson, andAndy Wilson.

Thomas M. Quigley

Editor

United StatesDepartment ofAgriculture

Forest Service

United StatesDepartment ofthe Interior

Bureau of LandManagement

Interior Columbia BasinEcosystem ManagementProject

AbstractJames, Sam. 2000. Earthworms (Annelida: Oligochaeta) of the Columbia River basin assessment area.

Gen. Tech. Rep. PNW-GTR-491. Portland, OR: U.S. Department of Agriculture, Forest Service,Pacific Northwest Research Station. 13 p.

Earthworms are key components of many terrestrial ecosystems; however, little is known of theirecology, distribution, and taxonomy in the eastern interior Columbia River basin assessment area(hereafter referred to as the basin assessment area). This report summarizes the main issues aboutthe ecology of earthworms and their impact on the physical and chemical status of the soil. Thethree main ecological types of earthworms found in the basin assessment area are epigeic, endo-geic, and anecic. Each type has a different life history pattern, resource requirement, and ecologicalfunction. Effects of environmental and habitat variables in the basin assessment area on these threetypes are summarized. Key ecological functions of earthworms are presented in relation to the eco-logical types and habitats of earthworms in the basin assessment area. These key ecological func-tions include the effects of earthworms on soils, their role in nutrient cycling, and their relation toother fauna.

Distributions of earthworm species in the basin assessment area also are summarized. Although mostof the known species from the area are exotics from Europe, at least three species are native to theregion. Unpublished records indicate that there may be many more species that have either not yetbeen collected or for which descriptions have not yet been published. Both the possibility of discov-ering additional macrofaunal biodiversity and the precarious status of at least one known speciesargue for additional research on earthworms in the basin assessment area.

Effects of land use and management practices on earthworms are explored by examining research onsimilar human influences in other ecosystems as no research on these issues has been done in theWestern United States. Suggestions for land use and future research priorities are provided.

Keywords: Earthworm, Oligochaeta, Columbia River basin, soil biota, land management.

Contents

1 Introduction

1 General Earthworm Ecology

3 Native and Exotic Earthworms of the Basin Assessment Area

8 Management Issues

10 Research and Monitoring Priorities

11 Conclusion

12 References

Int roductionEarthworms (Annelida: Oligochaeta) are animportant but much neglected component ofecosystems. It has been said that we know moreabout the 2 kilograms of bird tissue flying overeach hectare than about the 200 kilograms ofearthworms working the soil of each hectare(Bouche 1977; numbers apply to temperateWestern Europe). Understanding the key role ofearthworms in many biogeochemical cycles andin soil development requires an understandingof the impacts of land uses and other human-caused influences on earthworms. This is partic-ularly true in relation to restoration of damagedsystems and to preventive maintenance to avoiddamage.

Along with the effects of earthworms on soildevelopment, decomposition, and nutrientdynamics are other important considerations:earthworms are eaten by small mammals andbirds; invasion of soil in the basin assessmentarea by exotic earthworm species has occurredin many locations and is probably ongoing;invasions occurring in locations previously freeof earthworms likely will alter nutrient cyclingpatterns, soil food webs, and potentially thediets of small vertebrates; reduction in ranges ofnative species is due to destruction of habitat,displacement by exotic species, or by a combi-nation of the two; and currently, not enough isknown about the native species to determinewhether they are threatened or endangered.

The intent of this report is to supply sufficientinformation about earthworm ecology in theeastern portion of the interior Columbia Riverbasin (hereafter referred to as the basin assess-ment area) to those who make managementdecisions and determine research priorities.This paper provides a brief review of earth-worm ecology, highlights their key ecologicalfunctions, and presents distributional and eco-logical data for both native and exotic earth-worms in the basin assessment area. Manage-ment implications and directions for futureresearch also are discussed.

General Earthworm EcologyEarthworms are segmented worms of the phy-lum Annelida, class Oligochaeta. About 4,300species are known, and many more may awaitdescription, including some in the basinassessment area. They differ in certain funda-mental characteristics of body plan and repro-ductive organ layout from their close relativesin the aquatic Oligochaeta. One basic require-ment of earthworms, closely tied to their aquaticancestry, is moist soil in order to remain active,because gas exchange is conducted through awater film on the integument (Edwards andBohlen 1996), and burrowing is easier in moistsoil. Earthworms influence the soil environ-ment, and that influence differs with the ecolog-ical niches of different species. More detail fol-lows about environmental influences and con-straints on earthworm populations, the effects ofearthworm activity on their ecosystems, and theecological differences among earthworms.

Environmental influences on earthworms—Three environmental factors, moisture, tempera-ture, and pH, plus food resource quantity andquality, are the most important influences onearthworm populations. Soil moisture affectsearthworm abundance, activity patterns, andgeographic distribution. Soil temperature influ-ences seasonal activity, limiting earthwormsduring warm and cold periods. Soil pH often iscited as a limiting factor on earthworm distribu-tions, as the best studied group, EuropeanLumbricidae, generally does not inhabit soilswith pH below 4.0. Quality and quantity of foodresource also influence earthworm abundance.

Soil climate determines the periods of earthwormactivity. Within a habitat type, variations in soilclimatic factors occur (because of slope, aspect,soil particle size distribution, and drainage char-acteristics), that result in variation in earthwormactivity period and earthworm abundance. Aforested habitat probably has a relatively bufferedsoil climate compared to the more exposedgrasslands and agricultural land. Grassland tem-perature and moisture regimes are probablymore extreme and could accentuate the effects

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of slope, soil properties, and other site charac-teristics. An agricultural cycle having long peri-ods of bare ground could further intensify theimpact of weather on earthworms.

Although the well-known Lumbricidae typicallydo not inhabit soils with pH below about 4.0,other taxa tolerate lower pH values, includingsome Pacific coast native species (pH 3.1 to5.0; McKey-Fender and others 1994), therebyindicating that soil acidity might be less limit-ing for certain earthworm species than for others.

Organic matter enters soil food webs from litterfall or from root deposition. Surface litter maybe fed on directly or after prior ingestion anddefecation by other detritivores. Dependence onthese sources of organic matter, which are dis-cussed later, differs by species. Quality oforganic matter differs greatly among plantsources and can affect earthworm populations.Organic matter may render the soil stronglyacid, could be rich in digestibility-reducing com-pounds, or could have a high carbon-to-nitrogenratio. These qualities tend to reduce earthwormpopulations.

Lack of organic matter is generally a significantlimiting factor for earthworms. The fact thatmost agricultural soils are depleted of organicmatter likely accounts for lower abundance ofearthworms in agricultural land or recentlyabandoned cropland.

Effects of earthworms on soils and organicmatter—Much is known about the effects ofearthworms on soil characteristics and nutrientavailability (see Edwards and Bohlen 1996, Lee1985). Soil structure is altered by the creationof macropores and macroaggregates. Soil pro-files may be mixed vertically. Forest floor litterlayers can be entirely consumed by earthworms.These structural alterations affect the environ-ments and resource bases of other soil fauna,alter the relative abundances of bacteria andfungi in favor of bacteria, and change the pat-terns of water and gas movement into and with-in soils. Nutrient mineralization is enhancedby earthworm activity, either by digestion,assimilation, excretion, and tissue breakdown,or indirectly through accelerated bacterial

attack on organic matter. All earthworm excretahave higher levels of available macronutrientsand cations than the material ingested (see Lee1985). Urine is a source of available nitrogen.Also body tissues readily decompose afterdeath. In addition to mineralization, chemicaleffects resulting from passage of soil organicmatter through earthworms increase availabili-ty of some soil mineral nutrients. Because ofthe impact and generality of these phenomena,earthworms often are considered “keystone”members of soil and litter decomposer commu-nities. To understand the effects of earthwormson their environments, three ecological typesof earthworms and how they affect soils differ-ently must be considered.

Ecological diversity among earthworms:definitions and functional roles—Three mainecological categories of earthworm are widelyrecognized: epigeic, anecic, and endogeic(Bouche 1977). Epigeic worms are typicallysmall, darkly pigmented, and reside in leaf litterlayers under the bark of decaying logs or inother concentrations of organic material. Theyhave high rates of reproduction and short life-spans. Anecics inhabit a permanent or semiper-manent deep vertical burrow and emerge atnight to consume relatively fresh plant detrituson the surface. These are the largest and longestlived earthworms. Endogeics live in the mineralsoil and consume organic matter within the soilor at the soil-litter interface. They are larger,less pigmented to unpigmented, have longerlifespans, and have lower reproductive ratesthan epigeic worms. All three types also con-sume mineral soil to varying degrees, with theendogeics being the greatest processors of min-eral soil.

Lavelle (1983) further divided the endogeic cat-egory into polyhumic, mesohumic, and oligohu-mic types. Polyhumic endogeics work on richersources of organic matter in the early stages ofdecomposition closer to the soil surface or atthe soil-litter interface. Lumbricus rubellus andpossibly Aporrectodea trapezoides are examplesof this type of earthworm, which is characterizedby moderate dorsal pigmentation and modestdevelopment of intestinal surface area. Intestinal

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structures that increase gut surface area aremost highly developed in the oligohumic endo-geics found deeper in the soil and feeding onmore decomposed organic matter. Intestinal sur-face area is least developed in epigeics andanecics. Mesohumic endogeics have little or nopigmentation, intermediate secondary develop-ment of intestinal surface area, and poorlydeveloped escape behavior. Feeding is on well-decomposed organic matter.

The diverse life patterns of the different ecolog-ical types of earthworms cause different func-tional roles or effects on the ecosystem of eachspecies. The preceding general overview of theeffects of earthworms on soils and soil processesshould be understood in the contexts of the dif-ferent ecological types of earthworms. The nextlevel of refinement of understanding would bespecies-specific knowledge of functional rolesof earthworms; this information, however, is notknown for any of the native species in the basinassessment area, thus ecological type is theextent of our discussion.

Epigeic earthworms, which are generally forestdwellers, likely serve the following functions:

• Organic matter comminution—Reducing thesize of organic matter particles during passagethrough the worm makes organic matter moreaccessible to digestive action by other decom-posers.

• Nutrient cycling—Earthworms digest organicsand thus mineralize some of the nutrientsbound in them.

• Soil structure modification—Burrowing anddefecating create soil structures significant(though the details are unknown) to other soilbiota. The soil structures created are hydrologi-cally significant, and soil water-stable aggrega-tion is promoted.

• Transfer of organic matter to the soil—Con-sumption of surface litter results in defecationin the mineral soil, particularly if worms retreatinto the mineral soil to avoid unfavorable cli-matic conditions in the litter.

• Food for other animals—Predators of earth-worms include small mammals, feral pigs,beetle larvae, centipedes, some flies, and birds.

Anecic earthworms transfer relatively fresh plantlitter from the surface to deep levels of the soil,thereby creating deep vertical burrows, whichenhance water infiltration. Other earthworm typescan contribute to these processes but generallydo not. Anecics also provide food resources toendogeic worms by depositing fecal organicmatter (or casts) into the soil where endogeicscan reach it.

Functional roles of endogeic earthworm aresimilar to those mentioned for the epigeicspecies, with the following modifications:

• Soil profile development or transfer of materi-als within the soil—Defecation within the min-eral soil will not always be at the same level asconsumption. Deposition of casts may occuron the soil surface, in which case mineral soilis being brought up to the surface, and uppersoil horizon material may be being depositedin the deeper strata.

• Soil carbon protection—Endogeic earthwormsproduce fecal pellets, which are water-stableaggregates, and within which soil carbon ispartially protected from oxidation. Althoughthe initial evolution of a cast includes a phasein which microbial respiration of soil carbon isenhanced, the long-term effect of the incorpo-ration of organic matter into casts is to slowthe oxidation of soil carbon (Lavelle and Martin1992). In this way, earthworms contribute tothe soil carbon sink.

With some basic knowledge of earthworm ecol-ogy, we can now consider the status of earth-worms in ecosystems of the basin assessmentarea, specifically their distribution and ecology.We also will discuss management priorities.

Native and Exotic Earthworms ofthe Basin Assessment AreaThe state of present knowledge—Presently,little is known about earthworms in the basinassessment area. Although much of the region is

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too arid to support earthworms, many habitatsdo have earthworms, both native and exotic.Lack of knowledge of native earthworm fauna,some of which may be endangered by habitatloss, is a cause for concern. Undescribedspecies are likely present in the region. Nothingis known of how native species contribute toecosystem processes in the basin assessmentarea, or of how they interact with other species,such as earthworm predators. On the otherhand, many exotic species occur in the basinassessment area, possibly altering previouslyworm-free soils and nutrient cycling pathways,competing with native species, and generallymodifying any processes linked to soil physi-cal or chemical properties.

The known distributions of earthworms in thebasin assessment area are shown in figure 1(Fender 1985, Gates 1967). Many of the distri-bution marks are tightly clustered because sev-eral species were found at one site; hence acluster is generally one site, not several neigh-boring ones. Published data on earthworms ofthe basin assessment area thus are based on alimited number of collection locations. Only asmall portion of the earthworm-inhabitablebasin assessment area has been surveyed.

Fender1 indicates that five native genera are rep-resented in the basin assessment area: Driloleirus,Drilochaera, Argilophilus, Arctiostrotus, andMacnabodrilus; however, only three specieshave been described. Driloleirus americanusis known from eastern Washington and west-ern Idaho. Driloleirus americanus may beanecic, based on its deep burrowing habits andlargely organic diet. Drilochaera chenowithen-sis is known from only one site along theColumbia River at Chenowith Creek, west ofThe Dalles, Oregon (McKey-Fender 1970).Argilophilus hammondi has been found at theChenowith Creek site and well to the south inthe Ochoco National Forest on the slopes of

Grant Butte in Crook County, in an open pon-derosa pine (Pinus ponderosa Dougl. ex Laws.)forest with sedges and grasses in the understory,and at an elevation of about 1600 meters(McKey-Fender 1970). These native generahave other species on the west side of theCascade Range. Argilophilus ranges well tothe south into California to the latitude ofRiverside, California (Wood and James 1993).

The factors that influence native species popu-lations are unknown. Only by assuming thatthey are comparable to those of other earth-worms can it be said that soil moisture, soiltemperature, organic matter quantity and quali-ty, and soil pH are probably the most importantfactors (Lee 1985). We have, however, alreadynarrowed the consideration to specific habitattypes; and those probably fall within the limitsof tolerance of most temperate zone endogeicearthworms.

Because much research has been done on theecology of European earthworm species, moreis known about the exotics than about the nativespecies of the basin assessment area. TheEuropean species Dendrobaena rubida and theeastern North American Bimastos parvus areepigeic. Eiseniella tetraedra (also native toEurope) has epigeic physical and life historycharacteristics, but it is semiaquatic. Bimastosparvus was found in Engelmann spruce-sub-alpine fir (Picea engelmannii Parry ex Engelm.-Abies lasiocarpus Hook. Nutt.) cover under logsand stones, whereas Dendrobaena rubida wasfound in a riparian area within agricultural land(Gates 1967).

Lumbricus terrestris (common name: night-crawler) is a European anecic species. It wasrecorded from two artificial environments, a lawnat the University of Idaho and in a roadside pic-nic area near Pocatello, Idaho (Gates 1967).

The native species Drilochaera chenowithensisand Argilophilus hammondi are probably endo-geic, based on the physical characteristics givenin McKey-Fender (1970). European endogeicspecies recorded thus far are Aporrectodeatrapezoides, A. tuberculata, Eisenia rosea,

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1 Personal communication. 1996. Fender, W.M. Soil BiologyAssociates, 835 Ashwood Avenue, McMinnville, OR 97128-6801.

Lumbricus rubellus, and Octolasion tyrtaeum.All these species are widely distributed in NorthAmerica because of human activity.

Habitat factors important to earthwormsinthe basin assessment area—Both the potentialroles of earthworms in basin assessment areaecosystems and the possible impact of manage-ment decisions on earthworms can be roughlypredicted by considering the habitat requirementsof the main ecological types of earthworms inrelation to the climates and vegetation covertypes of the basin assessment area. In additionto simple edaphic parameters and soil proper-ties, the age and species composition of specificvegetation types are important.

Soil pH level often is cited as a limiting factorto the establishment of earthworms in borealforests or other acid soils. If any of the higherelevation forests have this characteristic, earth-worms may be restricted from those sites. Thespecies present in the basin assessment area aremostly exotics with proven abilities to handlewide variations in soil conditions, such asAporrectodea trapezoides. The known nativespecies tolerant of acid soil are from the westslope of the Cascade Range. Within the basinassessment area, Argilophilus hammondi wascollected from two ponderosa pine sites of pH5.5 and 6.0, values tolerable to almost anyearthworm.

Epigeic earthworms require plant remains inearly stages of decomposition and typically livein accumulations of organic material such asforest litter layers. Some species such asDendrobaena rubida and Bimastos parvus arefrequently found in down woody material. Toharbor epigeic species, a forest stand musteither grow under conditions that permit devel-opment of a litter layer or be old enough toproduce down woody debris, or both. Leaf litterdepth must be sufficient to provide moistureretention in the lower layers of the litter betweenrains so the worms can feed on the litter. Threeto six centimeters of litter and humified organicmatter is a safe minimum. Because these worms

are so active, they can find deep litter accumu-lations and woody debris, provided the moistureregime is favorable.

Down wood of 10 centimeters diameter willhave sufficient bark and decomposing cambiallayers to support these worms. The stage ofdecay and species of tree, however, are important.Logs in contact with the ground and reachingthe state at which the bark is loose but not yetfalling off are most likely to harbor these worms.In eastern forests, log-dwelling species seemless likely to be encountered in down oak andconifer logs, and more often are found inspecies such as maple, birch, aspen, tulippoplar (Liriodendron tulipfera L.), and cherry.It is unknown whether any native epigeicspecies are in the basin assessment area and, ifso, whether any of them utilize logs.

Anecic species can live in forested or grassland-shrubland areas provided they can escape deepinto the soil when soil climate is outside theiractivity range. The only other known require-ment is sufficient quality and quantity of litterproduction to sustain earthworm growth andreproduction. Because this factor is stronglycontrolled by water availability, litter quality ismore likely to be an issue than litter quantity.

Endogeic species seem to have the broadesthabitat ranges. In the basin assessment area,endogeic species occurred in a wide range ofhabitats, including forests, savannah, grassland-shrubland (including exotic grass pasture andseral stages following cessation of agriculture),and cultivated land. The primary factors account-ing for the distribution of exotic species in thebasin assessment area are a combination ofaccidental introduction by humans and theavailability of sufficient moisture where theseaccidental introductions have occurred. In thebasin assessment area, native endogeics areprobably confined to higher elevations andriparian areas. They may be absent from someinhabitable areas because of historical geologi-cal and climatic conditions of different regionswithin the basin assessment area.

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Biogeography—The eastern portion of the basinassessment area contains diverse land forms,soils, and vegetation types, some of which har-bor earthworms. Distributions of native andexotic earthworms in the basin assessment areadepend on many historical factors in addition tothe general soil climatic requirements of earth-worms. Large-scale climate changes, vulcan-ism, and substrate evolution could affect thepresence or absence of native species inregions where current conditions are favorable.Human activity has had a tremendous impact,both by destroying habitat and by inadvertentlyintroducing exotic species.

Presently, there is insufficient published infor-mation to allow us to identify areas of highdiversity or endemism or to outline regionswhere past climate or geological influences areresponsible for earthworm absence from habit-able conditions. On the local scale, earthwormsin temperate zones generally show low within-site diversity, with three to six species per site.In topologically complex land areas, manyspecies have limited distributions, which leadsto high diversity among sites. For example, NewZealand has about 200 species of earthworms,but seldom are more than four found in any onespot (Lee 1959). Fender (see footnote 1) estimatesthe Pacific coast earthworm fauna to contain 80to 100 species, including many undescribedbasin assessment area species. Given the sizeand topographic diversity of the basin assess-ment area, a conservative estimate of the even-tual number of earthworm species there mightbe about 20.

Forest Service and Bureau of Land Managementlands, particularly the former, are likely to har-bor most surviving native earthworm speciespopulations in the basin assessment area. Interiorponderosa pine and Douglas-fir (Pseudotsugamenziesii Mirb. Franco) forests and other non-xeric habitats probably support the nativespecies. Forest Service and Bureau of LandManagement lands near f ishable streams orhuman settlements also may harbor exoticspecies. The Steens Range, bitterbrush areas,juniper stands, and sagebrush are thought to

lack earthworms (see footnote 1). Fender sug-gests that native species tend to favor fine-tex-tured soils, whereas European Lumbricidaespecies can more easily invade coarse-texturedsoils. This could possibly be related to theprevalence of human activity along watercourseswith their alluvial coarse soils.

Among land areas outside of Forest Service andBureau of Land Management land areas, ripari-an zones, privately owned grazing land, andtimber land are most likely to contain native andexotic earthworms; agricultural land, particularlydryland farms, is less likely to contain either.Earthworms have been recorded from siteswithin cover types shown in basin assessmentarea current vegetation cover type maps (Eyre1980, Hann and others 1997, Shiflet 1994),2

and where available, collection data from Gates(1967) and McKey-Fender (1970): SAF 206(Englemann Spruce-Subalpine Fir), SAF 210(Interior Douglas-Fir), SAF 213 (Grand Fir),SAF 218 (Lodgepole Pine), SAF 237 (InteriorPonderosa Pine); SRM 107 (Western Juniper,Big Sagebrush, Bluebunch Wheatgrass), SRM109 (Ponderosa Pine-Shrubland), SRM 110(Ponderosa Pine-Grassland), SRM 304 (IdahoFescue-Bluebunch Wheatgrass), SRM 607(Wheatgrass-Needlegrass); CRB 001(Agricultural land), CRB 002 (Mixed grass-agriculture-shrubland), and CRB 004 (Sub-alpine herbaceous). The following additionalvegetation cover types from Gates (1967) andMcKey-Fender (1970) likely could be inhabitedby earthworms: CRB 003 (Seral shrubland-regeneration), SAF 217 (Aspen), SAF 235(Cottonwood-Willow), SRM 103 (Green Fescue),SRM 306 (Idaho Fescue-Slender Wheatgrass),and SRM 402 (Mountain Big Sagebrush).

Sensitivity to disturbance and population trendsare unknown for all the native species. Collectiondata from Fender (see footnote 1) and McKey-

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2 Columbia River basin succession model, (CRBSUM) currentvegetation cover types map. 1996. On file with: USDA ForestService; USDI Bureau of Land Management, Interior ColumbiaBasin Ecosystem Management Project, 112 East Poplar Street,Walla Walla, WA 99362. Also available on line: www.basinemp.gov/spatial/.

Fender (1970, 1994), however, suggest that vir-tually any disturbance that alters vegetation orallows the entry of exotic species can possiblyreduce or eliminate native species populations.Because their observations are not based onexperimental manipulations, it would be diffi-cult to define what conditions would threaten orendanger native species. We also do not knowthe degree to which habitat disturbance andecological competition contribute to thereplacement process. More information on thisissue is presented in the next section.

The exotic species from Europe have achievedtheir current global temperate zone distributionbecause of their broad adaptability to differenthabitats and their resilience following disturb-ance. Populations likely are expanding in num-bers and geographic extent as movements ofindividual species (basically a diffusion process)and accidental transport by humans enlarge theoccupied territory.

Management IssuesBiodiversity concerns: preservation of nativespecies and alterations to the ecosystemcaused by exotics—The basin assessment areais inhabited by at least three native earthwormspecies belonging to three genera. All threeshould be of special concern. The giant earth-worm, Driloleirus americanus, was consideredfor inclusion in Wells and others (1983) becauseits habitat was threatened and its range wassmall. Current information suggests that it maybe a narrow endemic using a threatened habitat(shrubland sites with good soil). The collectiondata give little detailed information about habi-tat type. The three sites (near Pullman andEllensberg, Washington, and Moscow, Idaho[Fender and McKey-Fender 1990]) are locatedin what is now agricultural land, grassland, andshrubland (CRB 001, 002).

The other two native species, Drilochaerachenowithensis and Argilophilus hammondi,may be somewhat tolerant of habitat disturb-ance. Their type localities were on uncultivatedcanyon and surrounded by orchards (McKey-

Fender 1970). They therefore may be consideredmore likely to survive but probably still shouldbe given special attention. In particular, learningmore about their ranges and ecological flexibili-ty would enable land managers to determinewhether or not special measures are necessary.

This leads to another area of concern to landmanagers: invasion by exotic species. Exoticearthworm species present in the basin assess-ment area are (thus far) all of European originand are all members of the family Lumbricidae,with the exception of one species indigenous toAmerica (Bimastos parvus). This invasion is acause for concern for two reasons. First, thesespecies may be able to outcompete nativespecies. Replacement of native species byexotics has been observed in many parts of theworld, including northern California (Eisen1900), Illinois (Smith 1928), New Zealand (Lee1961), and South Africa (Ljungstrom 1972). Ingeneral, native earthworms are vulnerable tohabitat disturbance and invasion by exoticspecies (Kalisz and Dotson 1989). Large areasof intact habitat seem to be somewhat moreresistant to native species loss, though the long-term outcome is not known.

The second reason for concern arises in regionswhere native earthworms do not occur. Thisabsence may be for many reasons, such asglaciation, long dry periods, and isolation frompotential colonists by intervening deserts. Soiland litter development in the absence of wormsis different from that in soil inhabited byworms, particularly in forest ecosystems (forexample, Langmaid 1964). There may be corre-sponding differences in the nutrient cyclingdynamics, soil mesofauna, soil microfauna, andsoil microflora of worm-free and worm-inhabitedsystems.

Sich concerns have led to the following ques-tions: Do land managers wish to maintain worm-free areas in their natural state? Is it importantto maintain native species, or for larger purpos-es of sustainable land use, is any worm goodenough? Efforts to control the spread of exotic

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earthworms may be futile, and insufficient infor-mation exists about the relative ecologicalimpact of native and exotic species to allowdecisionmakers to make informed decisionsabout how to manage earthworm biodiversity.

Land uses, earthworms, and earthwormfunctions—The fundamental issue here iswhether or not the ecological functions of andbiodiversity concerns about earthworms are suf-ficiently important to shape management deci-sions. In some soil systems within the basinassessment area, earthworms function as key-stone organisims; as such, they merit inclusionwith other more conspicuous organisms. Wenow know that earthworm introductions alterpreviously worm-free soils and can potentiallycause various effects on other groups of soilbiota and on nutrient cycling processes. Vitaldata are lacking about biodiversity and aboutwhether certain species may be endangered,either from habitat alteration or from the intro-duction of exotics. We do not have experimentalevidence directed specifically at those basicmanagement questions for which earthwormdata could be relevant. For now, and as a stimu-lus for further inquiry, I have assembled somebasic information on the impacts of grazing,prescribed fire, and logging on earthworms.These three land uses or management practicesare widespread and economically important tothe region.

Grazing—Effects of grazing on earthwormsinclude at least three components. First, manuredeposition on the soil surface reduces availableleaf litterfall. Second, root death results fromgrazing, and thus rhizodeposition of detritus inthe soil is increased (up to a point). Third, live-stock can cause soil compaction, thereby mak-ing burrowing and feeding more difficult forearthworms.

Conversion of herbage to manure by cattlechanges the quality and accessibility of detritalmaterial for earthworms. What would have beenlitter is now partly predigested, may be toxic inthe short term, is clumped rather than dispersed,and is highly attractive to several other inverte-brates. James (1992) describes the response ofseveral earthworm species to bison (Bison

bison) dung pats in tallgrass prairie. Specieswith characteristics of polyhumic endogeics(including Aporrectodea turgida—present inthe basin assessment area) were attracted todung, whereas other endogeics were not. Othercategories of worms were not represented in thesystem.

Hutchinson and King (1980) examine the effectsof sheep stocking rates on soil invertebrate pop-ulations, and Seastedt (1985) and Seastedt andothers (1986) consider the impact of clipping ormowing on soil arthropods. In general, thesestudies showed a peak of abundance at moderateplant defoliation levels. The results, however,are not as clear with earthworms: Seastedt andothers (1988) are inconclusive, but Todd andothers (1992) found increased abundance ofsome species with increased mowing frequencybut no change (statistically insignificant declinesof biomass) for other species. Consequently, itseems that any assessment of the impact of vari-ous grazing management scenarios will have tobe case by case.

Soil compaction caused by animal activity(including humans) has variable effects onearthworm populations. Cuendet (1992) foundcontrasting effects of pedestrians on earthwormsin two forest types; whereas Pizl (1992) foundthat the farm machinery in orchards negativelyaffects all earthworms. Different ecological cat-egories of worms were affected to differingdegrees in each case. More specifically, cattletrampling has a blanket negative effect thatresults in a decline in earthworm populationbut is less intense on large-bodied earthworms(Cluzeau and others 1992). In this study, tram-pling was intense, such as would be found bygateways or at water sources.

All three effects of grazing considered hereshow variable effects by earthworm species orhabitat type or both. Endogeic species often suf-fered less than epigeics, and large species werealso less heavily impacted. Without furtherknowledge about native earthworms and thepresence or absence of earthworms in land sub-ject to grazing in the basin assessment area, it isof little use to speculate further.

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Prescribed fire— James (1988) describes theimpact of fire in Kansas tallgrass prairie onnative earthworm populations. The effect waspositive because fire allows more rapid warm-ing of the soil in spring, thereby stimulatinggrowth of grasses. In contrast, European speciesdeclined with burning, probably because theywere less able to tolerate the higher soil temper-atures on burned plots. Fire, as a managementtool, thus may be short-term neutral or positiveon native endogeic species where fire is a naturaland frequently recurring element of the ecosys-tem. If invasions by exotic species occur neartheir temperature tolerance limits under fire-suppression conditions, they may be pushedbeyond the limits in the postfire environment.Anything that removes a litter layer and downlogs could negatively impact epigeics. Additionalinformation more relevant to forest fires can befound in Abbot (1984, 1985), though the workwas done in jarrah forests of Australia.

Logging—The primary effects of tree removalon endogeic species seem to be in the soil cli-mate area, with surface and soil organic matterpools probably sufficient to carry them throughuntil second-growth plants become established.If selective cutting practices are adopted, thisimpact will be moderated. Dis-turbance causedfrom heavy equipment use may be the mostdeleterious (Schaefer and others 1990).

Epigeic species would be expected to suffermost from the loss of tree cover because thiswould make their preferred microhabitat lesshospitable and ultimately less abundant, withthe loss of annual leaf input. There may be ashort-term increase from slash left on site, but itis difficult to say if the microclimate wouldremain suitable for earthworm activity.

The previously mentioned land uses and themanagement practices linked to them willaffect earthworms. Considering that basinassessment area habitats likely to be inhabitedby earthworms are generally those with enoughprecipitation to support some sort of economi-cally driven land use, practical human activity,management decisions, and the fates of earth-worm populations could be strongly related in

the basin assessment area. Federal and privateland decisionmakers in this diverse region maychoose to incorporate earthworm ecology andbiodiversity parameters in the information usedin making management decisions.

Research and Monitoring PrioritiesComplete rectification of the lack of informationabout earthworms in the basin assessment areais probably beyond the budgetary and scientificinfrastructure resources (particularly the supplyof experts) available. The most critical researchneed is an inventory of the species present, par-ticularly the native species, and their geographicaldistribution. An inventory will simultaneouslytell us much about the distribution of exoticspecies in the basin assessment area. The un-processed collection information of Fender(see footnote 1) and McKey-Fender (1990)could be worked up, and survey efforts could bemade to extend their work. Another high priori-ty would be experimentally testing hypotheses ofthe mechanisms through which habitat distur-bance, exotic species invasions, and otherhuman-caused factors may affect native species.This should begin with those species potential-ly threatened both in the basin assessment areaand globally, such as Driloleirus americanus.The next priorities would be to learn moreabout the population densities, habitat require-ments, and general ecology of native species inthe basin assessment area. An equally impor-tant priority for the exotic species would beresearch into their effects on litter decomposi-tion, soil horizon development, and other soilinvertebrates in regions otherwise free of earth-worms.

Once the high-priority areas of research are cov-ered, a basis for deciding the next direction forearthworm research in the basin assessment areacould be determined. Native species existing asdense populations in particular vegetation typeshave a higher priority for process- and commu-nity-level investigation than species naturallyoccurring in low numbers. Integrated researchwith specialists on other basin assessment areabiota is highly desired. Interactions with fungi,or earthworms as food resources for vertebrates,

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are some examples where high-priority organ-isms in forest ecology and wildlife conservationwould be involved. Because little is knownabout the earthworms of the basin assessmentarea, research could begin on almost any one ofthe priorities.

ConclusionEarthworms, called “the intestines of the earth”by Aristotle, are important to soil processes,other soil biota, and soil hydrology. Althoughlarge areas of the basin assessment area are toodry to support earthworms, they have beenrecorded in various habitats. Both exotic andnative earthworm species exist in the basinassessment area. This report presents the basicecological information necessary to begin eval-uating the effects of land management practicesand conservation policy on earthworm popula-tions. In addition, the question of how torespond to the presence of invasive exotics hasbeen raised. Findings presented in this paperprovide a starting point, a source of hypothesesto be examined in future research efforts anddiscussions on ways to preserve our naturallandscapes and their inhabitants.

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