Animal Burrowing Attributes Affecting Hazardous Waste Management

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Animal Burrowing Attributes Affecting Hazardous Waste Management K. SHAWN SMALLWOOD* Consulting in the Public Interest 109 Luz Place Davis, California 95616, USA MICHAEL L. MORRISON Department of Biological Sciences California State University Sacramento, California 95819, USA JAN BEYEA Consulting in the Public Interest 53 Clinton Street Lambertville, New Jersey 08530, USA ABSTRACT / Animal burrowing is critical to the formation of soils and contributes to the interface between geological materials and organic life. It also influences the management of hazardous materials at nuclear waste facilities and else- where. For example, residues and waste products from the production of nuclear weapons are released onto the ground surface and within engineered burial structures. Soil biotur- bation has exposed radionuclides and other hazardous ma- terials to wind and rain, thereby risking inhalation and injury to humans and wildlife on and off site. Soil bioturbation can expand soil depths and spatial distributions of the source term of hazardous waste, potentially increasing chronic ex- posures to wildlife and humans over the long term. Ample evidence indicates that some of the large quantities of haz- ardous materials around the world have been released from soil repositories, where they have also contaminated and harmed biota. Key burrowing parameters influencing these outcomes include the catalog of resident species, and their abundance, typical burrow volumes (void space created by soil displacement), burrow depth profiles, maximum depth of excavation, constituents and structural qualities of exca- vated soil mounds, and proportion of the ground covered by excavated soil. Other important parameters include rate of mound construction, depth of den chambers, and volume of burrow backfill. Soil bioturbation compromised the integrity of some hazardous waste management systems using soil, but the environmental impact remains largely unknown. De- signers and operators of waste management facilities, as well as risk assessors, need to understand how burrowing animals influence hazardous waste storage. Animal burrowing has been recognized by ecologists and pedologists as playing a significant role in soil formation, erosion, and ecosystem function (Grinnell 1923, Taylor 1935, Hole 1981). Soils are largely defined by living constituents (Ricklefs 1990), among which burrowing animals play a significant role. Burrowing behavior combined with plant and fungal growth and physical processes, such as precipitation, heating, and drying, generates a turbulent soil layer between the underlying geological formations and the overlying atmosphere. The biologically driven mixing of materi- als in this layer is termed soil bioturbation. Mixing the ingredients from weathering of geological materials and accumulation of humus facilitates plant root growth and nutrient uptake. Surface biota also contribute to soil bioturbation by eventually serving as dead material for humus and by loosening soil with root growth, animal foraging, locomotion, and dust bathing. Moving soil is one of the principal ecosystem services provided by burrowing animals (Mielke 1977, Huntly and Inouye 1988). Pocket gophers (Thomomys talpoides) can keep the soils completely mixed in the 35 to 60-cm depth horizon (Hansen and Morris 1968). Gopher (Geomyidae) burrowing also creates void space, which allows water and plant roots to infiltrate to greater depths more quickly (Hansen and Morris 1968, Cadwell and others 1989, Smallwood and Geng 1997), serves to aerate soils, and serves as habitat for many fossorial animal species that did not create the burrow (Vaughan 1961). However, the behaviors of burrowing animals that are so critical to the terrestrial life-support system can conflict with modern hazardous waste management systems and can disturb improperly handled waste. Soil bioturbation complicates the management of hazard- ous wastes deposited on or in soils, especially when the waste managers view soils as inert, stable material. KEY WORDS: Burrowing; Environmental impact; Radioactivity; Risk; Soil bioturbation; Hazardous waste *Author to whom correspondence should be addressed. Environmental Management Vol. 22, No. 6, pp. 831–847 r 1998 Springer-Verlag New York Inc.

Transcript of Animal Burrowing Attributes Affecting Hazardous Waste Management

Animal Burrowing Attributes Affecting HazardousWaste ManagementK. SHAWN SMALLWOOD*Consulting in the Public Interest109 Luz PlaceDavis, California 95616, USA

MICHAEL L. MORRISONDepartment of Biological SciencesCalifornia State UniversitySacramento, California 95819, USA

JAN BEYEAConsulting in the Public Interest53 Clinton StreetLambertville, New Jersey 08530, USA

ABSTRACT / Animal burrowing is critical to the formation ofsoils and contributes to the interface between geologicalmaterials and organic life. It also influences the managementof hazardous materials at nuclear waste facilities and else-where. For example, residues and waste products from theproduction of nuclear weapons are released onto the groundsurface and within engineered burial structures. Soil biotur-bation has exposed radionuclides and other hazardous ma-

terials to wind and rain, thereby risking inhalation and injuryto humans and wildlife on and off site. Soil bioturbation canexpand soil depths and spatial distributions of the sourceterm of hazardous waste, potentially increasing chronic ex-posures to wildlife and humans over the long term. Ampleevidence indicates that some of the large quantities of haz-ardous materials around the world have been released fromsoil repositories, where they have also contaminated andharmed biota. Key burrowing parameters influencing theseoutcomes include the catalog of resident species, and theirabundance, typical burrow volumes (void space created bysoil displacement), burrow depth profiles, maximum depth ofexcavation, constituents and structural qualities of exca-vated soil mounds, and proportion of the ground covered byexcavated soil. Other important parameters include rate ofmound construction, depth of den chambers, and volume ofburrow backfill. Soil bioturbation compromised the integrityof some hazardous waste management systems using soil,but the environmental impact remains largely unknown. De-signers and operators of waste management facilities, aswell as risk assessors, need to understand how burrowinganimals influence hazardous waste storage.

Animal burrowing has been recognized by ecologistsand pedologists as playing a significant role in soilformation, erosion, and ecosystem function (Grinnell1923, Taylor 1935, Hole 1981). Soils are largely definedby living constituents (Ricklefs 1990), among whichburrowing animals play a significant role. Burrowingbehavior combined with plant and fungal growth andphysical processes, such as precipitation, heating, anddrying, generates a turbulent soil layer between theunderlying geological formations and the overlyingatmosphere. The biologically driven mixing of materi-als in this layer is termed soil bioturbation. Mixing theingredients from weathering of geological materialsand accumulation of humus facilitates plant root growthand nutrient uptake. Surface biota also contribute tosoil bioturbation by eventually serving as dead material

for humus and by loosening soil with root growth,animal foraging, locomotion, and dust bathing.

Moving soil is one of the principal ecosystem servicesprovided by burrowing animals (Mielke 1977, Huntlyand Inouye 1988). Pocket gophers (Thomomys talpoides)can keep the soils completely mixed in the 35 to 60-cmdepth horizon (Hansen and Morris 1968). Gopher(Geomyidae) burrowing also creates void space, whichallows water and plant roots to infiltrate to greaterdepths more quickly (Hansen and Morris 1968, Cadwelland others 1989, Smallwood and Geng 1997), serves toaerate soils, and serves as habitat for many fossorialanimal species that did not create the burrow (Vaughan1961).

However, the behaviors of burrowing animals thatare so critical to the terrestrial life-support system canconflict with modern hazardous waste managementsystems and can disturb improperly handled waste. Soilbioturbation complicates the management of hazard-ous wastes deposited on or in soils, especially when thewaste managers view soils as inert, stable material.

KEY WORDS: Burrowing; Environmental impact; Radioactivity; Risk;Soil bioturbation; Hazardous waste

*Author to whom correspondence should be addressed.

Environmental Management Vol. 22, No. 6, pp. 831–847 r 1998 Springer-Verlag New York Inc.

Excavated soil is vulnerable to forces of erosion on theground surface (Cole 1932, Black and Montgomery1991, Litaor and others 1996).

Prior to the passage of the Resource Conservationand Recovery Act (RCRA 1983: Sect. 1004[5], 42U.S.C.A. Sect. 6903), and other regulations for thedisposal of hazardous wastes in the United States andelsewhere (eg, OECD 1982), landfills and surface im-poundments were likely to have been inadequatelycovered after closure, providing little protection againstanimal burrowing. The amount and distribution ofhazardous waste remaining at shallow depths can beestimated using statistics on early handling, treatment,disposal, and knowledge of soil processes.

Following passage of RCRA, EPA surveys found that260 million tons/yr of hazardous waste were producedby 14,000 generators during the early 1980s (Westat,Inc. 1984). This waste was stored at 4000 regulatedfacilities, of which 1500 treated wastes and 430 at-tempted disposal. Disposal facilities injected 32 milliontons/yr deep underground, beyond the reach of burrow-ing animals. Even if only 0.1% of the remaining 228million tons/yr were stored improperly or leaked withinthe top meter of soil, then 228,000 tons/yr would beaccessible to burrowing animals.

Moreover, waste generators producing less than 1000tons/month were not included in this survey. Suchgenerators, thought to number as many as 500,000,generated as much total waste as the larger generators,according to EPA staff (c.f., The Conservation Founda-tion 1984). If these generators handled a significantfraction of their waste on site, as was the practice by thelarger generators who handled 96% by volume (Westat,Inc. 1984), then improperly stored or leaking hazard-ous waste may lie at depths accessible to burrowinganimals at thousands of sites across the United States.

Superfund sites, monuments to a careless past, alsorepresent a potential source of toxic materials acces-sible to burrowing animals. The EPA’s national prioritylist includes 1210 such sites (USEPA 1996), and othersites await evaluation. Even these highly managed sitescan be compromised if the design fails to includeconsideration of burrowing animals.

Soil bioturbation has been given relatively littleconsideration, despite the likely variety and magnitudeof impacts on waste management systems. In his reviewof the environmental fate of radionuclides, Price (1971)attributed radionuclide movement in the soil to chemi-cal processes and root uptake. Burrowing animals werenot considered a transport vector by Price (1971), or byWhicker and others (1990) for their pathway food-chainmodel. Little and others (1980) presented soil in aseparate ecosystem compartment from plants and ani-

mals around Rocky Flats Plant and tested hypotheseswithout any regard to the definitive linkage between soiland biota. However, understanding the magnitude andnature of containment degradation requires some knowl-edge of the type of waste management system.

McKenzie and others (1986) predicted the impacton waste management systems due to soil bioturbationat the Hanford Nuclear Reservation in south-centralWashington State. They used the BIOPORT model,which was adapted from the more general BIOTRANSmodel developed to estimate theoretical losses of spentnuclear fuel stored underground. For the impacts ofanimal burrowing, McKenzie and others (1986) esti-mated for each species their burrow volume in cubicmeters per hectare per year, maximum burrow depth,proportion of burrow within 0.5-m depth intervals, andproportion of new burrows per hectare per year. McKen-zie and others (1986) identified this set of animalburrowing parameters of BIOPORT as contributingmuch more to surface radionuclide concentrationsthan the plant root intrusion parameters, rate of wastepackage degradation, concentration ratios of radionu-clides in the soil, depth and volume of soil overfill, soilerosion parameters, and succession rate.

However, BIOPORT estimates were based on incom-plete subsets of available research reports and errone-ous assumptions. For example, McKenzie and others(1986) represented the burrow attributes of northernpocket gophers at Hanford with those of Pappogeomyscastinops, which is a small gopher that constructs verysmall burrows in Florida (Hickman 1977). McKenzieand others (1986) also averaged one to three densityestimates per species. Averaging density was inappropri-ate because density can increase .1000-fold from low tohigh as the spatial extent of the study area is reducedfrom the largest to smallest reported in the literature(Smallwood and Schonewald 1996). Not all the residentburrowing species were included, and no distinctionswere made in burrow parameters among soil conditionssuch as backfill, edge, and overlying vegetation. De-tailed influences of animal burrowing are also missingfrom the available wind suspension models (Smith andothers 1982). BIOPORT provided a reasonable begin-ning for assessing the impacts of animal burrowing, butit needs to be improved with greater detail in burrowparameters and greater thoroughness in data collectionand synthesis.

The primary objective of this study was to reviewevidence that animal burrowing at hazardous waste sitescontributes significantly to environmental contamina-tion and degradation of waste management systems.Documented evidence is largely associated with radionu-clides, perhaps because they are easily detected. Our

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secondary objective was to describe animal burrowingattributes needing quantification for the design andmanagement of hazardous waste facilities, as well as formore rigorously assessing risks of vertical and lateraltransport of hazardous waste materials from their in-tended or last known soil horizons. We will relate theseattributes to each other and present a model useful forrisk assessment purposes and for improving BIOPORT.Some of the burrow attributes we will describe wereidentified during Smallwood and Morrison’s multiplevisits to Hanford Nuclear Reservation and Rocky FlatsPlant (near Denver, Colorado) during the discoveryphases of two large legal actions directed at the nuclearweapons complex. Although focused on the radioactiveand chemical hazards present at these two weaponsfacilities, the burrow attributes discussed in this paperare relevant to management of hazardous waste facili-ties of any type and size where wastes are buried orsurface soil contamination has occurred. We hope tocontribute to a research program directed towardsatisfactory characterization of soil bioturbation so thatburrowing animal and plant responses to waste manage-ment systems can be anticipated and incorporated intoplanning. Detailed examples of release estimates usingour proposed models will be presented in a subsequentpaper.

Impacts on the Environment

Leaks, dumping, and nuclear bomb detonationshave certainly contaminated the environment withhazardous materials. Whicker (1973) and Antonio andothers (1992) found plutonium in northern pocketgophers, deer mice, and thirteen-lined ground squirrels(Spermophilus tridecemlineatus) out to .1 km downwindof leakage onto the ground at the Rocky Flats Plant.Bradley and others (1977) found dose rates of littlepocket mice (Perognathus longimembris), kangaroo rats(Dipodomys microps and D. merriami) and four species oflizard (Callisaurus dracondoides, Cnemidorphus tigris, Scelo-porus magister, and Uta stansburiana) to increase whereplutonium was more concentrated in soil on the NevadaTest Site. Cattle, rabbits, and rodents downwind ofnuclear facilities and nuclear bomb detonation siteshave been contaminated due to inhalation (Romneyand others 1970, Smith and Black 1977, Smith andBernhardt 1977).

Hazardous waste has also escaped into the environ-ment outside its storage facilities. Shrub-to-ground for-aging birds accumulated ‘‘dangerous’’ levels of radionu-clides around waste ponds at Oak Ridge NationalLaboratory, Tennessee, due to ingestion of contami-nated invertebrates (Willard 1960). Cotton rats (Sigmo-

don hispidus) also accumulated 137Cs along the shores ofa waste pond at Oak Ridge (Garten 1979). Arthur andothers (1986) found radioactive dose rates of deer mice(Peromyscus maniculatus) and kangaroo rats (Dipodomysordii) to be functions of burrow depth, time spent belowground, depth of back-filled soil cap, and the amount ofradioactive material buried at the Idaho National Engi-neering Laboratory (INEL). Some of these animalsencountered lethal doses of radioactivity at INEL (Arthurand others 1986). Miera and Hakonson (1978) studieddose rates of wild populations of four small mammalspecies inhabiting a low-level liquid waste receiving areanear Los Alamos National Laboratory (LANL). Theyfound the species to vary in 137Cs dose rates, withgreater doses occurring on the less mobile speciesnearest the areas with greatest soil burden. Many casesof radioactive contamination in wildlife were discoveredat Hanford (Johnson and others 1994).

Contamination by radionuclides and other hazard-ous materials affected the distribution and abundanceof species populations. Petal (1980) found reductionsin colony density, colony size, and average body massamong ants (Lasius spp. and Myrmica spp.) subjected togreater concentrations of ground-deposited coal dustand metals in Poland. French and others (1974) foundthrough field experimentation that irradiated femalesof several reptile species became sterile when exposedto 0.04 Gy/day. Heteromyid rodents also showed in-creased sterility and reduced survival, but they had anincreased birth rate. O’Farrell and others (1972) foundsimilar sterility and mortality patterns among pocketmice (Perognathus parvus) irradiated with a dose of 5–11Gy. In some cases, contamination zones might becomesources of frequent genetic mutations and ecologicalsinks.

If waste sites serve as ecological sinks, then popula-tion turnover rates might be higher than normal due toreplacement by subadult dispersal (O’Farrell and oth-ers 1975, Boer 1981), as observed in ant colonies inPoland (Petal 1980). Rodent biomass is higher on theburied radioactive waste sites than off these sites (Grovesand Keller 1983, Gonzales and others 1995), makingpredators more likely to be abundant. Coyotes (Canislatrans) and badgers (Taxidea taxus) commonly excavateburrows of fossorial rodents on buried waste sites(Smallwood 1996a). A radioactively contaminated coy-ote scat containing skeletal remains of a pocket gopherwas found east of the BC cribs on the Hanford NuclearReservation in 1973 (O’Farrell and Gilbert 1975).Other contaminated coyote scats have been reported,and animal remains not described to species werefound in contaminated scats of coyote, hawks, and owls(e.g., Johnson and others 1994). Badgers digging in the

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BC cribs contaminated black-tailed hare feces across a15 km2 area and raptor feces out to 9.7 km away(O’Farrell and Gilbert 1975). The ecological commu-nity exacerbates hazardous waste contamination bybioaccumulating hazardous materials and complicatingcharacterization of its fate (Price 1971).

Animal burrowing has been generally associated withupward movement of radionuclides at Hanford (Mixand Winship 1993, Johnson and others 1994). Soilbioturbation is the most likely explanation for thefrequent and widespread discovery of radiological con-tamination on surface soils continuing to this day. Of101 buried waste sites ranked for waste mobility during1990–1992, 87% were identified as having problems(Mix and Winship 1993). Twenty-one of these sites wererated as having a history of spreading contamination, 18showed evidence of biouptake or contamination begin-ning to ‘‘move around,’’ 28 were rated as having a20%–50% chance of migration or uptake by plants oranimals, and 21 were rated as having a 10% chance ofmigration or uptake by plants or animals. Contami-nated soil particles are frequently found on and aroundHanford buried waste sites and are recorded withoutany transport pathway identified (Westinghouse Rad-rover Survey reports from 1995, TMA Hanford Radio-logical Survey Record for 1995, ERC Radiological Sur-vey Record for 1995). These contaminated soil speckswere likely transported from burial structures due tosoil excavation by northern pocket gophers, harvesterants (Pogonomymex owyheei), and other burrowing ani-mals. Johnson (1984) found 150 spots of contaminationon and around harvester ant mounds at a buried crib,216-B-55. These ant mounds have since been a source ofconstant problems, despite frequent application ofcontrol measures (Steve McKinney personal communi-cation 1996).

The continued discovery of many contaminatedanimals at Hanford indicates that soil bioturbation incontaminated soils has a significant environmentalimpact (Westinghouse Hanford Company QuarterlyEnvironmental Radiological Survey Summaries for 1995and 1996). Following Smallwood’s discovery of manygopher burrows atop waste burial structures at Hanfordduring June 1996, Hanford personnel captured andtested a gopher from the perimeter of 218-W-4 buriedwaste trenches. This first gopher sampled had 89/90Srconcentrations three orders of magnitude greater thanin surface soils of the waste management zone (Small-wood 1996a), indicating the potential for fossorialanimals to be contaminated with soil-entrained hazard-ous materials.

Considering the overwhelming evidence of contami-nation on and downwind of hazardous waste manage-ment zones, we found it remarkable that no genetic

studies or rigorous animal population studies have beenconducted at the nuclear waste sites across the UnitedStates. Population studies have been conducted only onthe controlled properties long distances away from thewaste management zone. Therefore, the environmentalimpact of the interaction between soil bioturbation andhazardous waste in soils remains largely unknown. Theimpact on human health and the quality of theirenvironmental resources also remains little known.Understanding and using animal burrow attributes toassess the magnitude of exposure will lead to improvedknowledge of how and to what degree hazardousmaterials at waste sites pose risks to human health andecological health issues, such as frequency of geneticmutations, birth defects, and mortality of functionallyimportant individuals within species’ populations.

Impacts on Waste Management Systems

Soil bioturbation can obviously disturb and abeterosion of hazardous material that lies unprotected dueto the improper practices of the past. Soil bioturbationcan also degrade the integrity of intentionally buriedwaste storage systems (Hakonson and others 1982),exposing hazardous materials to fossorial animals, theirpredatory and commensal associates, and downwindanimals including humans. Mound soils from animalburrows are highly susceptible to wind suspension(Figure 1) due to their fine texture and loosenedparticles that are elevated above grade (Murray 1967,Litaor and others 1996).

Animal burrowing and consistent erosion patterns(e.g., wind patterns) can also concentrate previouslydispersed hazardous materials in soil (Essington andothers 1977), thereby increasing observed variability inconcentrations (Poet and Martell 1972) and toxicity.For example, soil mounds excavated by pocket miceaccumulated radionuclides on a backfilled waste pondat Hanford (Paine and others 1979), and tunnel en-trances of prairie dogs and ground squirrels emitted thehighest levels of radioactivity from uranium mill tailings(Shuman and Whicker 1986). Plant litter and animal-excavated soils eventually cover previously excavated orsurface-deposited hazardous materials. Contaminatedsoils are transported downward when entrained inanimal fur or ingested along with plant roots and laterexcreted below ground. Contaminated litter can becarried below ground to nest chambers. Burrows alsocollapse, bringing contaminated soil and litter into thetunnels, which are later covered over and repaired bythe burrowing animal. Pocket gophers transportedsurface-deposited 137Cs to soil depths .30 cm (themaximum depth sampled) on buried waste structures atLANL (Gonzales and others 1995). These waste materi-

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als that migrate below ground are protected from forcesof erosion until burrowing excavates them to thesurface once again. Soil bioturbation likely releases thesoil-entrained radionuclides chronically as contami-nated soils are brought to the surface and suspended inwind and water.

Hazardous wastes enter the soil layer via two majorpathways: (1) deposition onto the ground from atmo-sphere and water; and (2) intentional burial. Hazardouswastes have been purposely and accidentally releasedinto the atmosphere from stacks of process facilities,burn pits, spray and mist, and into holding ponds.These releases mostly occurred prior to the RCRA of1975. These dispersed materials settled on the soilsurface in concentrations and locations that dependedon the dispersal methods used, the chemical and

morphological properties of the wastes, weather pat-terns at the time of the release, and topography andvegetation. Hazardous wastes also were spilled andpurposely sprayed or dumped onto the ground. Asignificant fraction of the material would have beenretained in the top meter of soil, where it was mostvulnerable to soil bioturbation, plant shoot growth,animal traffic, dust bathing, etc. This soil layer wasintended to be the waste repository, although some siteswere planned for remediation involving soil removal orcover. Prior to and sometimes despite remediation, allof these deposited materials can be suspended in windsor runoff following precipitation and moved laterally toother deposition sites, or they can be leached into soilby precipitation or covered by soil mounds excavatedfrom animal burrows.

Figure 1. Soil mound of thirteen-linedground squirrel (Spermophilus tridecemlinea-tus) on Trench T-11 at Rocky Flats Plant,Colorado, 20 August (top photo) and 10October 1996 (bottom photo). By 11 No-vember, the mound soil was completelyremoved by winds. The trench containedradioactive waste. Photos by K. S. Small-wood.

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Surface-deposited radionuclides have been docu-mented to resuspend in wind and move off the man-aged site (e.g., Poet and Martell 1972, Krey 1976, Littleand others 1980, Ibrahim and others 1996). Accord-ingly, soil depth distributions of ground-deposited radio-nuclides have changed at the Nevada Test Site (Hakon-son and Johnson 1973, Hakonson and Nyhan 1980), theRocky Flats Plant (Webb and others 1993), and at theHanford Nuclear Reservation (Rickard and others1988). For example, environmental media were sampledfor plutonium on study plots downwind of the RockyFlats 903 Drum Storage Area during 1972–1974 (Littleand others 1980) and again during 1989 (Webb andothers 1993) and 1993 (Ibrahim and others 1996).During these 16–20 years, the plutonium inventorydecreased 79% in the top 21 cm of soil and 93% in theplant litter (Webb and others 1993), although Ibrahimand others (1996) reported no change in the verticaldepth profile of plutonium within the soil. During thissame time, Zeis and Coonfield (1976) reported 63% peryear increases in plutonium concentrations in soils 1.6km off-site, and 46% per year increases at 3.2 km off-site.We conclude that the only reasonable mechanism formoving the level of plutonium from the top 3 cm ofon-site soil to off-site was soil bioturbation combinedwith wind entrainment. That is, the deposited radionu-clides were redistributed by burrowing animals so thatsome blew downwind and some were transported togreater depths below the ground surface (Figure 2).Hakonson and Nyhan (1980) found a similar majorreduction in plutonium from the upper soil horizon atthe Trinity Site after 23 years, and some of this pluto-nium moved down to depths of at least 30 cm. Hakon-son and Johnson (1973) reported the recurrence ofplutonium on the ground surface at Trinity Site nearly

20 years after $15 cm of clean soil had been spread atopthe contaminated surface layer. They also reportedheaviest animal tissue burdens in the lungs, which theyconcluded to have been caused by inhalation of wind-suspended plutonium. Essington and others (1977)concluded that the original depth profile and spatialdistribution of plutonium at the Nevada Test Site hadbeen obliterated by animal burrowing.

Intentional burial is another pathway for hazardouswaste materials to enter the soil layer. During the early1980s, 19 million tons/y were going into surface im-poundments (USEPA 1983), such as reverse wells, cribs,French drains, and trenches, many of which wereimproperly lined prior to 1975. Additional waste wasgoing into another 180,000 surface impoundments notlarge enough to qualify for the national survey. Another3 million tons/yr were going into landfills (USEPA1983), which had been generally unregulated as tohazardous waste disposal in past years. Holding pondsand their service ditches also, have been drained andcovered with soil (backfill or overfill). Soil has beenpiled upon stacks of barrels containing waste products,burn pits, and spill sites. Most soil overfill was reportedlyabout 8–26 cm deep on surface contamination (Owenand Steward 1973), and most backfill on trenches andlandfill range from 15 cm (Johnson and others 1994) to120 cm deep (Owen and Steward 1973). All of thesedepths keep the waste horizon accessible to at leastsome of the resident burrowing species at every wastemanagement site. Every hazardous waste site where soilis used for waste storage also has resident burrowinganimal species. Soil overfill actually attracts burrowinganimals to buried trenches containing cable and wire(Connolly and Landstrom 1969) and to buried wastesites (Gonzales and others 1995). Animals also excavate

Figure 2. Illustrated example of chang-ing hazardous waste profile in soil due tosoil bioturbation. The density of the pat-tern depicts the density of the hazardousmaterial in the soil.

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greater volumes of soil and burrow to greater depths inoverfill than in mechanically unaltered soils (Landeenand Mitchell 1981, Arthur and others 1987, Reynoldsand Laundre 1988).

Pocket gophers, harvester ants, and other species ofburrowing animals currently burrow into the soil over-fill of every buried waste structure examined by Small-wood at the Hanford Nuclear Reservation and RockyFlats Plant (Smallwood 1996a,b), and they also burrowinto the buried waste overfill at Los Alamos NationalLaboratory (Gonzales and others 1995) and IdahoNational Engineering Lab (Arthur and others 1987,Reynolds and Laundre 1988), into uranium mill tailingsin Wyoming (Shuman and Whicker 1986), and intocontaminated soil embankments at Oak Ridge (Garten1979). All of these waste sites contain radioactive materi-als, most of which are products of the nuclear weaponsindustry. Badgers excavated large holes into buriedwaste trenches in pursuit of gophers and ground squir-rels at Hanford, beginning the spread of radionuclidesacross a large geographic area (O’Farrell and Gilbert1975). At the Rocky Flats Plant, Smallwood (1996b)discovered a badger burrow extending right throughthe center of the overfill on trench T-9 (Figure 3), whichcontained dried sanitary wastewater treatment plantsludge, scrap metal and junk, perhaps flattened drums,and possibly other materials as well (DOE 1992). Thesludge contained total long-lived alpha activity of 14–133 Bq/g, which was buried under 0.6 m of soil cover(DOE 1992). The ground had subsided across much ofthe trench, especially around the badger burrow en-trance, around which was strewn scrap hardware previ-ously buried in the trench (Smallwood 1996b). Soiloverfill not only fails to protect hazardous wastes from

biointrusion, but actually might exacerbate the prob-lem. Unless properly covered and sealed off afterclosure, both surface impoundments and landfills wouldbe vulnerable to animal burrowing. Even a small frac-tion of improperly closed disposal facilities would leadto enormous quantities of hazardous material beingavailable for animals to disturb and bring to the surface.

Some burials include caps of asphalt, concrete,tephra, cobble, or intensively engineered biobarriersconsisting of layers and combinations of materialsdesigned to prevent intrusion of the waste by plant rootsand burrowing animals (Adams and others 1981, Geeand others 1995). Concrete and asphalt caps have shortlife-spans and require frequent maintenance (Adamsand others 1981). For example, the asphalt pad atRocky Flats, known as the 903 Pad, covers the local areawhere Krey (1976) estimated 37–41 3 1010 Bq (10–11Ci) of plutonium leaked from barrels of contaminatedcutting oil. The 903 Pad has been repaired twice sinceits 1969 establishment, and currently it has plantsgrowing through cracks and animal burrows extendingunder its surface (Smallwood 1996b). Moreover, ani-mals use the hard surfaces of containment structures toestablish nest chambers (Wheeler and Wheeler 1963),thereby possibly accessing the waste and abetting ero-sion of the barrier. Many hard materials meant toprotect sensitive equipment are readily penetrated bygophers, especially soft metals such as lead and alumi-num (Connolly and Landstrom 1969). Gophers couldtherefore infiltrate at least some buried waste contain-ers, and some of this waste material would likely beactively sought and transported to den chambers for useas nesting material (Connolly and Landstrom 1969).

Biobarriers are in use and under further develop-

Figure 3. Badger burrow extending di-rectly into Trench T-9 at Rocky Flats. Con-taminated machine parts were reportedlyburied in the trench, and some were appar-ently excavated by the badger. Photo by K.S. Smallwood.

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ment at Hanford and elsewhere because other barriersand soil overfill have failed to prevent intrusion byburrowing animals (Adams and others 1981, Gee andothers 1995). A prototype biobarrier, 200-MB1, wasconstructed over crib 216-B-57 at the Hanford NuclearReservation after intensive research and great expense.Smallwood visited this biobarrier in August 1996. Justprior to inspection, he was assured by the supervisingmanager of the biobarrier that no animals had yetburrowed on the biobarrier cap, based on the lastseveral years of intensive monitoring (also see Gee andothers 1995). Nevertheless, the inspection turned uptwo harvester ant mounds and evidence of numerousrodent burrows on the biobarrier cap (Smallwood1996a). Originally, biobarriers were being designed fora minimum effective 300-year life-span (Adams andothers 1981), but the targeted life-span has increased to1000 years (Gee and others 1995) and 10,000 years(Cadwell and others 1989). All these life-spans are toobrief to be considered the ‘‘ultimate disposal’’ of radio-active wastes.

Despite best efforts, shallow waste burials and surfacedeposits of hazardous materials remain vulnerable tomovement into the surrounding environment due tosoil bioturbation. Soil bioturbation can conceivablypressure the waste management systems, resulting insignificant loss of control over the environmental fate ofhazardous materials. The great expense and increasinguse of biobarriers are indicative of the challenge thathazardous waste managers encounter from soil bioturba-tion. However, no soil-barrier system has been proven toprovide satisfactory protection from plants and burrow-ing animals. Serious quantitative research efforts andpolicy recommendations are warranted by the humanand ecological health risks posed by animal burrowingand plant growth on hazardous waste sites. Animalburrowing needs to be better understood by risk asses-sors and by designers and operators of waste manage-ment facilities.

Burrowing Attributes for Estimating Impacts

To estimate the impacts of burrowing animals on therisk of environmental exposure from nonvolatile chemi-cals and radioactive elements at waste managementsites, it is helpful to characterize the waste distributionin the soil and the management system. It is also helpfulto: (1) catalog the burrowing animal species that occurat the waste site and to estimate their (2) densities(abundance per unit area), (3) average and maximumburrow depths, (4) proportion of burrows within depthhorizons, (5) rate of soil excavation to the groundsurface, and (6) characteristics of the excavated soil,

such as texture, particle size distribution, and structuralfate. Other burrow attributes can aid in making theseestimates, such as mounds produced per animal peryear, mound volume, average burrow volume, andspecies analogs (information for species taxonomicallyand functionally similar to those for which informationis lacking). To estimate the risk of exposure to soil-borne hazardous materials among burrowing animalsand their commensal neighbors and predators, it isnecessary to catalog the commensal and predatoryspecies that share or invade the burrow, obtain anaverage and range of den chamber depths, and estimateaverage home range sizes of the burrowing species andtheir commensal and predatory associates.

Some nonburrowing attributes also need to be con-sidered to assess risk, including the need to sample theburrowing animals for tissue burdens of the hazardoussubstance(s) and for symptoms of contamination, sam-ple the soils in the mounds and burrow for concentra-tion levels of the hazardous waste materials, and samplefrom the commensal animal species that regularlyreside in the burrow or the predators that regularlyconsume individuals of the burrowing species. Theseattributes will need to be characterized by directedprograms of research. The remainder of the paper willdescribe in greater detail the burrowing attributesuseful for assessing impacts. Representation of eachattribute in a predictive model is presented in thesection ‘‘Rate of Soil Excavation.’’

Catalog of Species

The first step in considering the potential and realimpact of soil bioturbation at hazardous waste sites is toidentify the plant and burrowing animal species thatreside at the site or perhaps previously resided at thesite. Different species of burrowing animals behave verydifferently, and each uniquely influences soil move-ment, void space, soil constituents, and locations wherebioturbation and related erosion will occur. For ex-ample, deer mice (Peromyscus spp.) excavate shallowburrows with small-diameter tunnels, whereas prairiedogs (Cynomys spp.) excavate much deeper burrowswith much wider tunnels. Prairie dogs also constructstrong, weather-resistant mounds from a mix of sur-rounding soil and vegetation scraped into the mound,whereas deer mice create small, loose piles of soil withno intended purpose except to get the soil out of theway. There are many other differences, as well. Even asingle species can vary dramatically in burrowing behav-ior from place to place. Therefore, the species and thelocal behaviors need to be cataloged.

Burrowing animal species that could have previouslyresided at the site also need to be considered, even

K. S. Smallwood and others838

though little or no evidence of their presence might beobserved today. For example, Townsend ground squir-rels (Spermophilus townsendi) were reportedly abundantacross the Hanford Reservation (Fitzner and Gray1991), but Smallwood (1996a) found no evidence ofthese squirrels during three site visits. Similarly, pocketgophers were reportedly abundant across the RockyFlats Plant (Murray 1967, DOE 1980), including on fourstudy plots within close proximity of the 903 Pad (Littleand others 1980, Winsor and Whicker 1980). However,Smallwood (1996b) found less than the expected abun-dance of gophers on the Rocky Flats Plant, especiallygiven the high abundance he found just off the plantproperty. The conspicuous rarity of these species atthese sites warrants consideration of whether they wereharmed by the hazardous materials managed there.

Burrowing animal species that no longer occur at ahazardous waste site might also have succumbed to thehazardous materials or to intensive control efforts.Black-tailed hares declined sharply in abundance in thevicinity of Hanford’s BC cribs, where radioactive fecesmarked their former presence (O’Farrell and Gilbert1975). Many animal species are affected by hazardousmaterials in the same or similar manner as humans(Gough and others 1977). Unlike humans, however,burrowing animals at a hazardous waste site live most orall of their lives exposed to the hazardous materials atthe site. A conspicuous absence of a burrowing animalspecies could indicate that the environmental impact ofthe site has already occurred. Alternatively, animalspecies are naturally clustered across their range (Small-wood and Schonewald 1996), and these clusters shiftlocations through time (Koford 1958, Taylor and Taylor1977, Boer 1981). The species population that shouldoccur at a hazardous waste site according to range mapsmight occur nearby just because the population shiftedlocations a few years previously. Its impact on thehazardous waste management system could have beenfelt while one of its clusters coincided with the site formany years. Prairie dog towns regularly expand andcontract and shift locations through time (Koford1958). Only a few years of prairie dog burrowing on ahazardous waste site would be necessary to dramaticallychange the spatial and vertical distributions of thehazardous materials. Species that likely declined at thesite should be included in the catalog for subsequentimpact assessments.

Animal Density

After cataloging the burrowing animal species at thesite, population density is critical for assessing levels ofsoil bioturbation. The number of individuals per unitarea is one of the most important influences on esti-

mates of annual burrow volume per unit area andpercentage of ground covered by excavated soil mounds.However, animal density is meaningless without beingdefined on spatial and temporal scales (Smallwood andSchonewald 1996). In addition to resolving density tothe spatial scale of interest and season of the year,density needs to be predicted separately for mechani-cally unaltered soils, backfilled soils, and edge condi-tions. Most population density estimates for burrowinganimal species have been made on agricultural andnatural soil conditions, but population density of burrow-ing animal species can increase on backfilled soilscovering waste trenches, ponds, ditches, and landfill.The vertical and near-vertical walls of waste trenchesand ditches offer vertical and lateral edge, which isoften sought by burrowing animals (Criddle 1930,Boone and Keller 1993). Active trench walls can beinfiltrated and riddled with tunnels prior to burial,thereby predisposing these waste structures to lateranimal burrowing (Smallwood 1996a,b). Hard coverssuch as asphalt and concrete slabs can attract burrowinganimals along their edges due to the lateral edge andweather-proofing over constructed den chambers(Wheeler and Wheeler 1963). Research will be neededto estimate multipliers for densities of species inhabitat-ing backfilled and edge soils.

Animal density is important because the excavatedburrow volume will be needed to assess the impact ofsoil bioturbation. Animal density can range .100-foldfrom low to high density (Smallwood and Schonewald1996), whereas the average burrow volume might range10-fold from low to high volumes among studies for asingle species. If animal density of a species reportedlyvaries from 1 to 100 individuals/ha, and if burrowvolume per individual varies from 0.05 to 0.5 m3/yr,then the product of density and burrow volume canyield 0.05–50 m3/ha/yr, a 1000-fold range of uncer-tainty mostly due to the uncertainty in density. Much ofthe observed variation in density is due to differences inspatial scales of observation by the researchers who haveestimated density, so spatial resolution of density isneeded to reduce the uncertainty range of burrowvolume per unit area per year. Defining density tospatial area can be accomplished using regressionanalysis on the available density estimates reported forthe species:

log (density) 5 a 1 b 3 log (study area).

Burrow Depth

The depth of burrows typically constructed by cur-rent and past species must be known to assess impactsfrom soil bioturbation. These animals are capable oftransporting surface-deposited materials to the depths

Burrowing in Hazardous Waste 839

of their burrows, which can significantly alter the costsand feasibility of waste cleanup. These animals can alsotransport buried waste to the ground surface so long asthey can burrow deep enough to infiltrate contami-nated soil and buried waste. Boxes and barrels of wastecan be used as convenient den chambers by burrowinganimals. Other waste materials such as paper, cloth,rubber gloves, and packing materials can be trans-ported to nest chambers for use as nesting materials.The heat generated by radioactive wastes might alsoattract burrowing animals to greater depths than typi-cally achieved, so some excavations of animal burrowson buried waste structures should be made.

The greatest volume of animal burrowing occurswithin the top half meter of soil, so surface-depositedmaterials are most vulnerable to vertical and lateralmovement due to soil bioturbation. The surface contami-nation at the 903 Drum Storage Area of Rocky Flats wascovered by 8 cm of soil overfill, which was less than theburrow depths of most if not all the resident burrowinganimal species. The overfill on many buried waste sitesusually varies from 0.15 to 1.23 m, and overfill on cribsat Hanford can be 2.46 to .3 m deep. The overfill ofmost buried waste sites is less than the typical burrowdepths of some resident species, and some species canreach the cribs at Hanford, although rarely. The likeli-hood of animal intrusion can be increased further whenthe soil overfill erodes away. Besides the typical depths,maximum burrow depth needs to be considered, be-cause a single intrusion into some buried waste sites canbe disastrous. Badgers and pocket gophers can reachburied cribs at Hanford, and prairie dogs can reachthose depths where they are found.

Burrow depths of Great Basin pocket mice (Perogna-thus parvus) increased in backfilled soils over a wastepond at the Hanford Nuclear Reservation. They in-creased their burrow depths 90% on the backfilled soilsas compared to nearby soils in shrub-steppe vegetation(Landeen and Mitchell 1981). These pocket mice alsotransported buried 137Cs in pond sediment to theground surface, with 20 times the activity level inmounds than in other surface soils. On another part ofthe Hanford Nuclear Reservation, harvester ants tun-neled through 3.7 m of backfilled soil and transportedplutonium from a broken pipeline to the groundsurface (Smallwood 1996a). Burrow depths need to becharacterized in natural and mechanically altered soils,as well as at sites with vertical edge (e.g., buried trenchwalls or containers).

Burrow Depth Profiles

Assessing the impact on the environmental fate ofhazardous wastes in soil requires characterization of the

proportion of the typical burrow within arbitrary depthintervals. If the hazardous material occurs within thetop 3 cm, then the amount attached to loosened soilparticles due to burrowing will be more for a speciesthat digs 15% of its burrow within the top 3 cm than fora species that digs 3% of its burrow there, so long as theburrow volumes are equivalent. The proportion ofburrow volume in each depth horizon needs to bemultiplied by the typical burrow volume to estimate thevolume of soil excavated from each depth horizon. Theusefulness of the predictions improves with the use ofsmaller depth intervals, but as the depth interval isreduced, the sample size of burrows needs to beincreased. Burrow depth profiles are critical for estimat-ing the impact of burrowing animals on the soil-entrained hazardous wastes.

Rate of Soil Excavation

The typical burrow volume per species is central toany assessment of soil bioturbation impacts. Oncedescribed satisfactorily, burrow volume can be multi-plied by animal density and the proportion of newburrows per year to estimate the cubic meters of soilexcavated per unit area per year from burrows of thatspecies. The cubic meters per hectare per year ofexcavated soil per depth horizon for every burrowinganimal species resident at the site can be summed for atotal at each depth horizon. The depth profile of soilexcavation rates can then be compared with the depthprofile of the hazardous materials to predict impact.The burrowing rate profile can also be used to estimatethe impact on soil overfill by considering the propor-tion of loosened soil likely to move off-site every yeardue to local erosion forces, and the proportion ofnon-eroded contaminated soil covering the surfacelayer. The erosion rate of soil overfill is useful forestimating the remaining overfill depth (lacking directmeasurement due to health hazard or lacking permis-sion), thereby allowing an annual shifting in estimateddepth profile of the hazardous materials.

Ideally, burrow volume also needs to be character-ized separately for natural versus backfilled soils, andwithin different soil types and environmental condi-tions. It is best estimated by carefully excavating, map-ping, and measuring burrows. Typical burrow volumescan also be determined by multiplying typical tunnelcross-sectional area by tunnel length and adding thevolume of the typical number of den and food-cachechambers. Burrow volumes also can be estimated indi-rectly by monitoring the amount of soil brought to theground surface, although this would require monitor-ing throughout the year and allows only crude character-ization of burrow depth profiles.

K. S. Smallwood and others840

The rate of soil excavation also depends on thenumber of burrows constructed per animal per year.The role of animal density in calculating soil excavationrates also needs to be adjusted by the number of animalsoccupying each burrow. A single animal per burrowrequires no adjustment of density, but three animals perburrow per year would require density to be multipliedby 0.33 prior to multiplication with typical burrowvolume. For each of s species, the rate of burrowconstruction, BR (cubic meters per hectare per year),can thus be predicted from the following model:

BRs 5 BV · m1m2(D)

where BV is the typical burrow volume (cubic meters)measured by excavated soil; D is the density (number ofindividuals per ha); m1 is the multiplier of density basedon number of individuals per burrow per year ornumber of burrows per individual per year; and m2 isthe multiplier of density due to effect of soil backfill andedge relative to surrounding, mechanically unalteredsoil (e.g., magnitude of attraction to soil overfill or toedge of hard substrate, Figure 4).

The alternative burrow excavation rate can be esti-mated by integrating burrow dimensions:

BRs 5 BVt · m1m2(D)

where BVt 5 At · Lt 1 nd (dv) 1 nf (Fv), and At is thetunnel cross-sectional area (square meters); Lt is thetunnel length (meters); nd and nf are the number of den

and food-cache chambers; dv is the den chamber vol-ume (cubic meters); and Fv is the food cache chambervolume. All of these terms can and should include errorterms.

Burrow depth profiles can be constructed using thefollowing model:

BRi 5 BRs · pi · m3

where Bri is the rate of burrow construction in the ithdepth horizon, pi is the proportion of the burrow withinthe ith depth horizon, and m3 is the multiplier of BRs

and pi due to the effects of soil backfill or edgeconditions on species s. Burrow depth profiles growmore useful for assessing impact on hazardous wastemanagement and on the environment as the depthintervals are narrower (e.g., every 10 cm rather thanevery 50 cm used in BIOPORT).

Characteristics of Excavated Soil

Excavated soil can reveal concentrations of hazard-ous materials being displaced, the amount of contami-nants on the ground surface being covered by soil,chemical properties of the soil that might influenceplant growth and water infiltration, and possible ero-sion rates. All of these soil characteristics can influencethe environmental fate of the hazardous materials insoil. Water infiltration could leach contaminants out ofthe reach of plant roots and burrowing animals, whichis the purpose of cribs. Water infiltration can also leachthe contaminants into the groundwater aquifer, wherelateral movement can take the contaminants to otheraquifers, lakes, and streams used for drinking water.Wind erosion can involve saltation or long-distancetransport far off-site, depending on the size distributionand stickiness of excavated soil particles. The sizedistribution of eroded soil particles can also influencethe respirable fraction of excavated hazardous materi-als. Fine soil particles are more likely to be inhaled, andthe finest particles are most likely to pass toxins into thedeep portions of the lung, where most damage oftencan be caused. Animal burrowing exposes many of thefinest soil particles to wind.

Exacavated soil also varies in susceptibility to suspen-sion in wind depending on soil mound profile, the areaof cleared space around the mounds, and the topogra-phy upon which the animals prefer to burrow. Tallermounds are more likely to lose soil particles to wind.Harvester ants clear 1 to 3-m-diameter circular areas ofvegetation around their colonial mounds, which arepartly constructed by the clipped vegetation. This clear-ing further exposes the mounds to wind. Westernharvester ant (Pogonomyrmex occidentalis) mounds areoften constructed on prominent ridge tops or preci-

Figure 4. Illustration of typical distribution of a burrowinganimal species (e.g., gophers) in relation to buried hazardouswaste structures observed at Hanford Nuclear Reservationand Rocky Flats Plant (gopher density within dimensions ofHanford’s 216-B-12 crib is used as an example).

Burrowing in Hazardous Waste 841

pices of plateaus—places where wind is most likely toexert maximum force against the mounds. Many burrow-ing animals prefer soils with sparse vegetation, espe-cially on backfilled soils typical of hazardous wasteburial structures. Bulk density of backfilled soils isalready lower than mechanically unaltered soils, andwhen excavated onto the ground surface, bulk densitymight even be lower. Mounds on sparsely vegetated,backfilled soils are most susceptible to wind suspension.

Useful soil characteristics to be measured for assess-ing impacts on hazardous waste management systemsfrom soil bioturbation include concentration levels ofthe managed hazardous waste materials, as well as soilbulk density, soil moisture (infiltration rate), pH, con-ductivity, organic matter content, and concentrations ofnitrogen/nitrates, phosphorus, potassium, and cal-cium. Hazardous waste materials in soil mounds indi-cate animal intrusion into the waste horizon. Other soilcharacteristics may indicate likely physical and chemicalinteractions between the soil, the waste, and the sur-rounding environment. They can also indicate likelysuccessional patterns. Soil should be sampled for thesecharacteristics and measured from within excavatedmounds at various heights from grade to the moundtop, from burrow tunnel walls at depth intervals to thedeepest portion of the sampled burrows, and fromsurrounding soils at the same depth intervals. Soilbackfill within tunnels (backfilled by burrowing animal)should also be sampled. This sampling protocol wouldprovide more direct measures of impact from soilbioturbation.

The percentage of ground surface covered by animal-excavated soil can be used to estimate the amount ofsoil annually suspended in winds and moved by rain,once the weather patterns have been characterizedadequately. The ground covered by excavated soil is alsoprotected from wind and rain until the cover is erodedaway. This variable can therefore be used to estimatepart of the rate of downward migration of surface-deposited hazardous materials. It can also be used toestimate the number of years before some fraction ofthe surface-deposited hazardous material is covered byclean soil, thereby converting acute resuspension tochronic resuspension. This estimate needs to includeconsideration of the rate of spatial shifting of animalburrows. For example, animal burrows that remain inthe same location every year will pile soil mounds oneupon the other in the same places and might nevercompletely cover the ground surface with excavatedsoil. Characteristics of excavated soil have not beenrepresented quantitatively in models used for risk assess-ments of exposure.

Surface Excavation

Not all animal excavation of soils is a result of burrowconstruction. A substantial proportion of top soil isdisplaced every year by animal dust bathing, foragingand food-caching, daily sheltering, and locomotion(Smallwood 1996b). Dust bathing by rabbits, hares,rodents, and other animals can loosen the top severalcentimeters of soil comprising patches of 0.2–0.5 m2.Rodents and birds store food just under the groundsurface. Many species of arthropods, reptiles, and am-phibians burrow into the ground every day to escapeheat, cold, or predators. Deer hooves and the feet ofother animals punch holes in the soil and kick it upevery time they move across the landscape. A compre-hensive assessment of soil bioturbation impact willrequire estimates of the percent of ground disruptedand the volumes of soil moved due to the above-groundactivities of terrestrial animal species. This type ofimpact will be most substantial where contaminantswere deposited on the ground surface, and it has yet tobe represented quantitatively in risk assessments ofexposure.

Commensalism Among Fossorial Animals

Spatially shifting clusters of resident burrowing ani-mal species also tend to cluster together (Koford 1958,Campbell and Clark 1981). Often, where one species isfound, so too are many of the others. Burrowinganimals readily make use of burrows made by otherspecies, by rotted tree roots, and by human construc-tion and soil management activities. As more tunnel isexcavated, more opportunity becomes available forburrowing animals. For example, pocket mice at Han-ford burrow right into gopher mounds, and an activetrench wall at Hanford was burrowed into by nestingbank swallows (Riparia riparia), which were later at-tacked by a badger after barrels of waste were stackedunder the nest holes thereby giving the badger access(Figure 5). Even after these trenches are filled, the largecavities in the soil constructed by the badger canfacilitate future burrowing to greater-than-usual depths(Davis and Kalisz 1992).

On mechanically unaltered soils on arid landscapes,where waste management zones are often located,burrowing animals are often attracted to clumps ofrelatively lush vegetation. The coincidence of animalburrows and lush vegetation is well documented (Rog-ers and Lavigne 1974, Davis and Kalisz 1992, Smallwoodand Geng 1997), including at the Rocky Flats Plant(Antonio and others 1992). Burrowing facilitates plantgrowth, which is targeted by burrowing animals for foodand cover. After long time periods, the topography ofthe landscape can reflect the clustering of animal

K. S. Smallwood and others842

burrowing. Nonrandom accumulations of soils due toanimal burrowing are the leading hypotheses for theformation of mima mounds (Cox 1990) found acrossthe Hanford Plateau and pimple mounds found acrossRocky Flats (Murray 1967). Harvester ants also accumu-late particular soils by covering their mounds withequal-sized soil granules (Wheeler and Wheeler 1963).These areas of concentrated burrowing should alsoconcentrate the movement of soil-entrained hazardousmaterials. The prominence of these mounds, and theirfine texture and loose arrangement of particles makemound soils highly susceptible to suspension in winds(Murray 1967, Litaor and others 1996), and thereforewarrant serious study.

Magnitude of Burrowing Impacts

As part of a scoping exercise to identify the relativeexposure risks posed by multiple release pathways,Smallwood (1997) used the above models to estimate 52m3/ha/yr of soil was excavated to the ground surface byburrowing animal species on Hanford’s buried wastesites. His estimate was six times the estimate of 8.88m3/ha/yr using the BIOPORT model (McKenzie andothers 1986), thus illustrating the effects of morethoroughly using the available information. Assumingno repair of the waste caps, the burrowing animalscould infiltrate the waste packaging, and the plutoniumwas uniformly distributed within the waste horizon,Smallwood (1997) used our models to also estimate thatburrowing animals excavated 13,246 GBq (358 Ci) ofplutonium to the ground surface from five Hanfordwaste sites during 1970–1996, or 1.8% of the 737,447GBq (19,931 Ci) of the plutonium inventory in those

sites (Maxfield 1979). Assuming the wind suspends halfof the excavated surface soil, he estimated 6623 GBqmoved off-site in respirable form, which was 100 timesgreater than the total amount of plutonium estimatedby Heeb and others (1996) to have been released intothe atmosphere by Hanford’s four separations plantsduring operations. These five waste sites contained only32%–58% of the plutonium in soils conceivably avail-able to burrowing animals (Maxfield 1979), so wind-suspended plutonium due to soil bioturbation mighthave involved 11,433–20,683 GBq during these 26 yearsat Hanford, so long as all the sites had similar soiloverfill and waste packaging. This magnitude of releaseamounts to 12–22 times the 930 GBq of plutoniumestimated to have leaked from drums of contaminatedwaste oil onto the soil at Rocky Flats Plant (Mongan andothers 1996), an accidental release that led to consider-able concern and investigation (e.g., Poet and Martell1972, Krey 1976, Zeis and Coonfield 1976, Little andothers 1980, Winsor and Whicker 1980, Webb andothers 1993, Antonio and others 1992, Ibrahim andothers 1996).

Conclusion

Soil bioturbation is a strong and critically importantforce of nature that should be considered in developingevery hazardous waste management system that usessoil. The impact of soil bioturbation was grossly underes-timated and undermitigated for buried and surface-deposited radionuclides and nonvolatile chemicals andmetals at Hanford Nuclear Reservation and Rocky FlatsPlant, where animal burrowing continues to excavateand spread the wastes (Smallwood 1996a,b, 1997).

Figure 5. A badger enlarged the nest bur-rows of barn swallows on an active nuclearwaste trench, 218-W-4A, at Hanford (Small-wood 1996a). Photo by Joe Wayman.

Burrowing in Hazardous Waste 843

Other researchers also found soil bioturbation respon-sible for moving hazardous waste materials at otherwaste management facilities (e.g., Garten 1979, Arthurand others 1987, Shuman and Whicker 1986, Gonzalesand others 1995). The impact of soil bioturbation hascaused serious problems for conventional hazardouswaste management systems, which have failed to pro-vide the necessary protection against intrusion andtransport of wastes by burrowing animals.

Large quantities of radionuclides, nonvolatile chemi-cals, and toxic metals will require containment andintensive management for many thousands of years atlocations around the globe. To avoid hazards created byfuture waste storage and to remediate existing shallowwaste burials and contaminated ground surfaces, wastesite managers need estimates of biological intrusionand transport rates at various depth horizons, down-ward migration rates due to soil bioturbation andleaching, wind suspension rates, and subsequent expo-sure risks. They will need to know of the soil manage-ment practices that can attract burrowing animals.Research is needed to improve our knowledge of theinfluential burrowing attributes we discussed in thispaper. Burrows constructed by multiple animal speciesneed to be measured and their soil excavation ratesmonitored in various soil conditions sampled acrosstheir geographic ranges. Burrows and their inhabitantson hazardous waste sites should be sampled for thehazardous materials stored, spilled, or leaked there, soas to directly measure their impacts. Excavated soilmounds that vary in particle size distributions need tobe monitored to characterize wind suspension rates andtransport distances. Furthermore, the magnitude of soilbioturbation needs to be characterized for species ofsoil invertebrates and microorganisms. Our discussionof burrow attributes only scratches the surface inaddressing the consequences of storing or depositinghazardous materials on or in soil, which is an ecologi-cally active medium.

Acknowledgments

We thank Joe Wayman for ideas and donating manylabor-intensive hours in the field. We also thank thepersonnel of the Hanford Nuclear Reservation, RockyFlats Plant, Los Alamos National Laboratory, and Dr.Larry Cadwell for their cooperation. We thank KevinGuse, Andrea Erickson, Brian Smallwood, and BrendaNakamoto for their assistance. We thank Steve Forrestand an anonymous reviewer for helpful comments onan earlier draft of this manuscript.

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