a modified risk assessment to establish molybdenum standards for land application of biosolids

REVIEWS AND ANALYSES

A Modified Risk Assessment to Establish Molybdenum Standardsfor Land Application of Biosolids

George A. O’Connor,* Robert B. Brobst, Rufus L. Chaney, Ron L. Kincaid, Lee R. McDowell,Gary M. Pierzynski, Alan Rubin, and Gary G. Van Riper

ABSTRACT provided by biosolids (O’Connor and McDowell, 1999).Similarly, rangelands—the predominant land use in theThe USEPA standards (40 CFR Part 503) for the use or disposalarid and semiarid western regions of the USA—offerof sewage sludge (biosolids) derived risk-based numerical values forabundant acreages for land application of biosolids.Mo for the biosolids → land → plant → animal pathway (Pathway

6). Following legal challenge, most Mo numerical standards were Aside from providing plant nutrients and enhancing soilwithdrawn, pending additional field-generated data using modern bio- conditions, land application of biosolids can increasesolids (Mo concentrations �75 mg kg�1 ) and a reassessment of this plant cover, decrease runoff, and reduce erosion (Drae-pathway. This paper presents a reevaluation of biosolids Mo data, ger et al., 1999). Pastures and rangelands also typicallyrefinement of the risk assessment algorithms, and a reassessment of represent low-population areas that minimize aestheticMo-induced hypocuprosis from land application of biosolids. Forage problems and traffic issues associated with biosolids use.Mo uptake coefficients (UC) are derived from field studies, many of

Biosolids, however, also contain trace elements whosewhich used modern biosolids applied to numerous soil types, withfate must be considered in pasture and rangeland im-varying soil pH values, and supporting various crops. Typical cattleprovement programs involving land application. In 1993,diet scenarios are used to calculate a diet-weighted UC value thatthe U.S. Environmental Protection Agency (USEPA)realistically represents forage Mo exposure to cattle. Recent biosolids

use data are employed to estimate the fraction of animal forage (FC) promulgated regulations (40 Code of Federal Regulationslikely to be affected by biosolids applications nationally. Field data [CFR] Part 503) that, coupled with state regulations, gov-are used to estimate long-term Mo leaching and a leaching correction ern biosolids recycling (USEPA, 1994). The federal rulefactor (LC) is used to adjust cumulative biosolids application limits. is risk-based (to protect against reasonably anticipatedThe modified UC and new FC and LC factors are used in a new adverse effects), and assesses exposure of animals, hu-algorithm to calculate biosolids Mo Pathway 6 risk. The resulting mans, and the environment to biosolids-borne metalsnumerical standards for Mo are cumulative limit (RPc) � 40 kg Mo

through 14 pathways. One of the assessment pathwaysha�1, and alternate pollutant limit (APL) � 40 mg Mo kg�1. We regardpertinent to biosolids use on pastures and/or rangelandsthe modifications to algorithms and parameters and calculations as(Pathway 6) evaluates metal transfer from biosolids →conservative, and believe that the risk of Mo-induced hypocuprosissoil → plants → animals. Exposure to molybdenum (Mo)from biosolids Mo is small. Providing adequate Cu mineral supple-

ments, standard procedure in proper herd management, would aug- via Pathway 6 is critical because ruminants (especiallyment the conservatism of the new risk assessment. cattle) grazing forage containing excessive Mo can de-

velop a Mo-induced Cu deficiency known as molyb-denosis. Pathway 6 was, by far, the limiting pathway forMo in land application programs, and calculations ofApplication on agricultural land is the most common

beneficial use of biosolids today (National Re- allowable biosolids Mo loads to soils from the pathwaywere used to set numerical standards for Mo in thesearch Council, 1996), and pastures frequently represent

attractive application sites. For example, pastures in federal rule. The next most limiting pathway was Path-way 3 (direct human consumption of soil), and yieldedFlorida occupy �5 million ha, are frequently underfertil-

ized, and respond well to nutrients (e.g., N, P, S, Fe) a Mo limit �20-fold greater than Pathway 6. Four tablesin the Part 503 rule define various types of pollutantlimits: Ceiling Concentrations in Table 1, Cumulative

G.A. O’Connor, Soil and Water Science Dep., and L.R. McDowell, Pollutant Loading Rates in Table 2, Pollutant Concen-Dep. of Animal Science, Univ. of Florida, P.O. Box 110510, Gaines-

trations in Table 3, and Annual Pollutant Loading Ratesville, FL 32611. R.B. Brobst and A. Rubin, USEPA, 401 M St., SW,in Table 4. Molybdenum was included in all tables, withWashington, DC 20460. R.L. Chaney, USDA/ARS, Beltsville, MD

20705. R.L. Kincaid, Dep. of Animal Sci., Washington State Univ., numerical values of 75 mg Mo kg�1 (Table 1), 18 kg MoPullman, WA 99164. G.M. Pierzynski, Dep. of Agronomy, Kansas ha�1 (Table 2), 18 mg Mo kg�1 (Table 3), and 0.9 kgState Univ., Manhattan, KS 66506. G.G. Van Riper, Montgomery Mo ha�1 yr�1 (Table 4).Watson, Lakewood, CO 80228. Although employees of the USEPAwere involved in the preparation of this document, it has not had the

Abbreviations: BC, background concentration of pollutant in forage;USEPA’s peer and policy review, and does not necessarily reflect theFC, fraction of animal forage likely to be affected by biosolids applica-views of the agency. Contribution of the Florida Agric. Exp. Stn.tion; HEI, highly exposed individual; LC, leaching correction factor;Journal Ser. no. R-07599. Received 15 June 2000. *CorrespondingRF, allowable Mo increment in plant tissue; RPc, cumulative biosolidsauthor ([email protected]).application limit; TPI, threshold pollutant intake at which a toxic effectis noted in animals consuming the forage; UC, uptake coefficient.Published in J. Environ. Qual. 30:1490–1507 (2001).

1490

O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS 1491

Table 1. Summary of Mo analytical results from the 1988 nationalClimax Metals Company, and several other compa-sewage sludge survey of waste treatment plants (USEPA,nies engaged in Mo production, use, and processing 1990b).

activities, filed a petition with the United States CourtTreatment No. Percent Mean Standardof Appeals for the 10th Circuit seeking a review of theplant capacities samples detection concentration deviation

land application numerical limits for Mo. Petition reviewmg kg�1was subsequently transferred to the Washington, DC

�4.38 m3 s�1

Circuit Court. The litigants claimed that the data used (�100 MGD)† 26 69 8.08 6.10�0.438�4.38 m3 s�1in the critical pathway risk assessment were faulty, and

(�10�100 MGD) 61 77 12.98 17.18that the Mo numerical limits were, thus, overprotective�0.044�0.438 m3 s�1

of public health and the environment. Litigants also (�1�10 MGD) 70 66 10.31 11.05�0.044 m3 s�1claimed that the USEPA had disregarded the basis of

(�1 MGD) 42 48 8.89 17.54a previous rule (USEPA, 1990) banning the use of hexa- National 199 53 9.24 16.58valent chromium (chromate) as an algaecide in comfort

† MGD, million gallons per day.cooling towers. In the proposal to the rule, the USEPArecommended molybdate as a cost-effective and non- than offered here. Molybdenum toxicity (molybdenosis)toxic replacement for chromate (USEPA, 1988). The was first identified in 1938 as the cause of severe diar-USEPA agreed with the petitioners’ assertions, and sub- rhea and emaciation in cattle-grazing areas called teartsequently agreed to temporarily suspend the Mo numer- pastures in England. In the same reference, Fergusonical limits for Tables 2 through 4 of 40 CFR, Part 503, et al. (1943) reported that the problem could be cor-but retain the ceiling value of Table 1 (USEPA, 1994). rected by copper sulfate addition to diets. Clinical signsThe Agency committed to reconsider its risk assessment of a Mo-induced Cu deficiency in ruminant animals,of Mo, including evaluating new data pertinent to the such as cattle and sheep, are exacerbated by increasedeffects of biosolids Mo land application. The USEPA S in the diet. Severe Mo toxicity signs in cattle includecommitted to formulate, and propose for public com- debilitating diarrhea leading to emaciation, loss ofment, new Mo numerical standards for 40 CFR, Part weight, and sometimes death. Mild Mo-induced hypo-503 Tables 2 through 4 after this reevaluation (USEPA, cuprosis may be expressed by hair color changes (achro-1994). The USEPA expects to propose new Mo stan- motricia). A direct effect of Mo on animal reproductiondards in 2001, respond to public comments, and promul- has also been demonstrated (Phillippo et al., 1987).gate Mo standards for Tables 2 through 4 thereafter (A. Cattle appear to be the most susceptible species toRubin, personal communication, 2000). Mo toxicity, followed by sheep. Horses grazed the teart

This document represents the reevaluation of biosol- pastures of England with no clinical signs of Mo toxicity.ids Mo data and risk assessment. We begin with brief Differences in susceptibility among species are usuallyreviews of Mo sources and uses and Mo toxicity. We interpreted to suggest that processes in the rumen en-then address recent data for Mo in biosolids and, finally, hance the toxicity of Mo by reducing the availabilityconsider Mo risk assessment. The latter effort includes of Cu. However, ruminants like mule deer and goatsa review of the initial risk algorithms and their parame- tolerate up to 1000 mg Mo kg�1 diet, about the sameters, and updated databases pertinent to their use. We as chickens, rabbits, and rats (Ward and Nagy, 1977;then offer a new algorithm, and provide data for its use Anke et al., 1985).to calculate Mo numerical standards. No clear evidence of Mo toxicity has been reported

in humans (Frieberg et al., 1975), but Ward (1994) rea-Sources and Uses of Molybdenum soned that human tolerance would be expected to be

much higher than for cattle or sheep, as is the case forMolybdenum was not described chemically until theall nonruminant species studied.late 18th century, but its use had been documented as

Copper intake is the primary interaction factor inearly as the 14th century (International MolybdenumMo toxicity because sufficient Cu supplementation canAssociation, 1999). Steel and cast iron production is thecounteract almost all disorders associated with high Molargest user (�75% of the Mo produced), but Mo is alsointakes (Clawson et al., 1972). Ward (1994) identifiedused in the manufacture and use of pigments, catalysts,dietary factors clearly related to Mo-induced hypo-lubricants, corrosion inhibitors, and fertilizer (Interna-cuprosis as Cu intake, Cu availability, S intake, Fe in-tional Molybdenum Association, 1999).take, and the physical form of the feed.Besides Mo in food and feces, the most common

Dietary Cu is poorly absorbed in most animal species,source of Mo discharged to sewer systems is from com-although absorption is greater in young than maturefort cooling towers, where water is used as a recirculat-animals and in Cu-deficient than Cu-sufficient animals.ing cooling medium in the towers. Chemicals are addedMature sheep absorb less than 10% of the Cu ingestedto control corrosion, mineral deposition, scaling, and(Suttle, 1973). Often, only 1 to 3% of dietary Cu is ab-bacterial and algae growth (Bastain and Brobst, 1993).sorbed in ruminants. The Cu availability in cereal grainsmay be 10 times greater than in forages (Suttle, 1986).Molybdenum Toxicity This partially explains why Cu deficiency can be a prob-

An extensive review of Mo requirements, toxicity, lem with grazing bovines, but usually not with dairyand nutritional limits for humans and animals (Ward, cattle or finishing cattle that receive greater amounts

of concentrates in their diets.1994) is recommended for those desiring more detail

1492 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001

Tab

le2.

Dat

aus

edto

esti

mat

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oup

take

coef

fici

ents

(UC

valu

es)

for

vari

ous

crop

s.

Stud

ySo

ilM

oT

issu

eM

oU

ptak

ety

pe†

Pla

nt,t

issu

eSo

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load

‡co

ncen

trat

ion

coef

fici

ent§

Ref

eren

ceC

omm

ents

kgha

�1

mg

kg�

1

For

age

nonl

egum

es

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rn,s

tove

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R¶

0–9.

70.

24–0

.67

0.04

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and

Bat

es(1

985)

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ched

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olid

sSo

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ads

calc

ulat

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itia

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load

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0–6.

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0–3.

70.

44A

NR

0–10

0.24

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80.

004

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enri

ched

bios

olid

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NR

0–12

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0.65

0.00

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oint

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mat

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0.24

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80.

003

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ched

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olid

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0.72

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term

plot

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tinu

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corn

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0.00

219

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13–0

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219

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0.21

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1997

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200.

13–0

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997

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age

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60–

0.65

0.51

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al.(

2001

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Exp

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trat

ion

each

year

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6.2–

6.6

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42–0

.51

0.00

1#19

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6.6

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00.

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ing

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eans

Aco

rn,s

tove

r6.

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3.0

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1977

,197

9,an

d19

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ter

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at6.

70–

2.0

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1.0

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taet

al.(

1999

)So

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ated

from

soil

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entr

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ns.

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and

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ads

calc

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ncen

trat

ion

each

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.(1

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pres

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ted

aver

age

over

seve

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ear

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(199

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Tab

le2.

Con

tinu

ed.

Stud

ySo

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issu

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pe†

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nt,t

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load

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trat

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1

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als

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0–9.

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0.01

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dB

ates

(198

5)C

a-en

rich

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ids

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load

sca

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ated

from

init

ial

bios

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ads.

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R0–

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ched

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001

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R0–

130.

25–0

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0.00

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n,gr

ain

4.6–

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14.3

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1.6

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and

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r1,

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al.(

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term

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load

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1).

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erim

ent

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leaf

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rzyn

ski

and

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(198

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6.6

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gree

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7.0–

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9

Con

tinu

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ge.


Copper bioavailability in forages is greatly influencedby forage levels of S and Mo and, to a lesser degree,by forage Fe, Zn, and Cd levels. In the presence of S,high intakes of Mo can induce a Cu deficiency due toformation of insoluble Cu–Mo–S complexes (e.g., thio-molybdates) in the digestive tract that reduce the ab-sorption of Cu (Mason, 1986, 1990). Several pathwaysexist by which Cu � Mo � S interactions mediate Cudeficiency (Dick, 1956; Ryan et al., 1987). Sulfur alsoexerts an independent effect on the availability of Cuto ruminants, and the effect of S alone may be greaterthan the S-dependent effects of Mo (Underwood andSuttle, 1999). Sulfides react with molybdate in the reduc-ing medium of the rumen to replace oxygen, producingthiomolybdates. These concepts of Mo–Cu antagonismin ruminants envisage that Mo acts, not by direct interac-tion with Cu, but as a secondary consequence of Moaffinity for sulfide generated within the rumen. Ex-cessive quantities of dietary S (�3 to 4 g kg�1 ) as sulfateor elemental sulfur may cause toxic effects and, in ex-treme cases, can be fatal (Kandylis, 1984). The effectsof soil ingestion and Fe excess on Cu absorption (Suttleet al., 1975; Suttle et al., 1984) are believed to resultfrom Fe binding of sulfide in the rumen, with subsequentrelease of sulfide in the intestine that interferes withCu absorption.

Most clinical signs attributed to the three-way interac-tion are the same as those produced by simple Cu defi-ciency and probably arise from impaired Cu metabo-lism. The tolerable risk threshold of Cu to Mo ratio infeed is not fixed, but declines from 5:1 to 2:1 as pastureMo concentrations increase from 2 to 10 mg kg�1 (Suttle,1991). Alloway (1973) suggests that the critical Cu toMo ratio is 4:1, whereas Miltimore and Mason (1971)suggest a narrower ratio of 2:1. Inclusion of S in theinteraction is preferable to use of only Cu to Mo ratios,but this consideration has not been reduced to a field-validated formula or ratio.

For grazing bovines, the problem of Cu deficiencydue to low forage Cu or a conditioned Cu deficiency(e.g., high forage Mo and/or S) is restricted to the usualsix-month season for grazing of green forages. The con-dition is rarely seen during the feeding of stored foragesin either beef or dairy cattle. Copper deficiency can behighly detrimental for cattle grazing fresh forage in someregions, but when this same forage is dried as hay, thereis no Cu deficiency (Huber et al., 1971; Allaway, 1977).These authors suggested that drying forage makes Cumore available for absorption and reduces the availa-bility of Mo.

Suttle (1980) evaluated Cu bioavailability of grazedpastures, dried grass, hay, and silage by responses inplasma Cu during repletion of hypocupremic ewes. Cop-per in cut hay and grass was more bioavailable than Cuin fresh grass and silage from the same field. Copperabsorption in fresh grass ranged from 0.5 to 2.8% inthree of the four grasses. Copper absorption was 0.9 to1.9% for grass silage, 3.1 to 4.9% for dried grass, and5.2 to 7.2% for hay.

Bioavailability of Cu is affected by the genetics of

Tab

le2.

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ruminants as well as antagonists such as Mo and S. There


Table 3. Base information used on the calculation of fraction of diet affected (FC).

Total Crop, Pasture, Total Biosolids Land Pasture Weighting WeightedStates in farms† pasture range pasture‡ produced§ required¶ affected# factor†† FC‡‡

Column

A B C D E F G H I J

103 ha 103 Mg 103 ha %AL 3 523 643 430 1 073 47 9 0.88 62 0.54AK 357 3 265 269 15 3 1.1 0 0.00AZ 10 873 47 9 584 9 631 43 9 0.09 100 0.09AR 5 813 813 593 1 406 28 6 0.39 60 0.24CA 11 210 504 5 821 6 326 720 144 2.3 77 1.7CO 13 207 284 8 071 8 355 60 12 0.14 100 0.14CT 145 11 8 19 83 17 88 26 23DE 235 4 2 7 22 4 66 100 66FL 4 231 362 1 647 2 010 253 51 2.5 100 2.5GA 4 319 438 332 770 274 55 7.1 42 3.0HI 582 17 364 381 17 3 0.90 14 0.12ID 4 788 330 1 857 2 188 32 6 0.29 100 0.29IL 11 010 334 273 607 474 95 16 89 14IN 6 115 251 147 399 297 59 15 89 13IA 12 613 810 583 1 393 98 20 1.4 100 1.4KS 18 652 1 390 5 691 7 081 100 20 0.28 100 0.28KY 5 396 1 255 456 1 712 47 9 0.55 18 0.10LA 3 188 340 407 747 60 12 1.6 60 0.97ME 490 26 11 38 19 4 10 89 8.9MD 872 60 39 99 172 34 35 100 35MA 210 16 10 26 203 41 160 33 52MI 3 995 195 76 271 402 80 30 47 14MN 10 520 404 383 787 47 9 1.2 90 1.1MS 4 097 455 378 833 45 9 1.1 100 1.1MO 11 666 2 124 1 504 3 627 250 50 1.4 53 0.72MT 23 718 651 15 368 16 019 10 2 0.01 38 0.00NE 18 424 745 8 853 9 598 64 13 0.13 100 0.13NV 2 594 105 2 118 2 223 39 8 0.35 36 0.12NH 168 9 6 15 18 4 25 48 12NJ 337 26 14 40 236 47 120 47 55NM 18 530 237 16 486 16 724 19 4 0.02 60 0.01NY 2 936 256 192 448 340 68 15 47 7.1NC 3 692 357 156 513 170 34 6.6 100 6.6ND 15 929 580 4 200 4 779 9 2 0.04 100 0.04OH 5 707 343 233 576 330 66 11 60 6.9OK 13 443 2 016 6 245 8 261 50 10 0.12 100 0.12OR 7 062 368 3 911 4 279 98 20 0.46 100 0.46PA 2 901 276 151 426 464 93 22 100 22RI 22 2 1 3 32 6 220 9 20SC 1 859 206 99 305 118 24 7.7 45 3.5SD 17 950 932 9 546 10 478 13 3 0.02 100 0.02TN 4 501 990 398 1 388 96 19 1.4 100 1.4TX 53 140 4 824 34 833 39 657 268 54 0.14 83 0.11UT 4 866 226 3 742 3 968 16 3 0.08 39 0.03VT 511 53 34 87 13 3 2.9 100 2.9VA 3 330 615 435 1 050 235 47 4.5 75 3.4WA 6 143 204 2 001 2 205 75 15 0.68 100 0.68WV 1 398 266 214 480 20 4 0.83 100 0.83WI 6 030 388 286 6 744 156 31 4.64 100 4.6WY 13 796 298 12 162 12 460 3 0.6 0 100 0US 377 092 26 089 16 017 186 706 6 856 1 371 0.73 81 0.59

† Hectares (ha) listed as acres and converted using 2.471 ha�1 in the 1997 agricultural census (USDA, 1999).‡ Total pasture in hectares (Columns C � D).§ Biosolids produced by state in Mg yr�1 in 1996 (Bastain, 1997).¶ Total hectares required if all of the biosolids produced in the state were applied to pasture at 5 Mg ha�1.# Percent of pasture if all of the produced biosolids in a given state were applied at 5 Mg ha�1 to pasture.†† Weighting factor is the percent biosolids land-applied in 1996, times 1.5 to a maximum of 100% of the biosolids produced.‡‡ Weighted FC based on biosolids that are land-applied in a state.

are marked variations within breeds in the efficiency of Underwood (1981) suggested that Mo is readily andrapidly absorbed from most diets. Hexavalent water-absorption of minerals from the diet, varying from 2 to

10% for Cu in adult sheep (Field, 1981). When different soluble forms, sodium and ammonium molybdate, andthe Mo of high-Mo herbage, most of which is waterbreeds of sheep grazed certain pastures in Scotland, one

breed exhibited signs of Cu poisoning, whereas another soluble, are particularly well absorbed by cattle (Fergu-son et al., 1943). Absorption of Mo from the disulfideshowed signs of Cu deficiency (Wiener and Field, 1969).

Goonerante et al. (1989) reported that Cu deficiency in (MoS2 ) is poor, owing to low solubility and the antago-nistic effect that S has on Mo absorption. MolybdenumSimmental cattle from Canada was more frequent than

in other breeds. Feeding high levels and combinations absorption depends on animal species, age, and level ofMo in the diet, but the average value is 20 to 30%of Cu, Mo, and/or S resulted in greatly enhanced biliary

Cu excretion in Simmental versus Angus cattle. based on experiments involving stable and radioactive


Table 4. Estimates of Mo leaching rates.

Study k Climate conditions

% Mo leached yr�1

Phillips and Meyer, 1993 1.86† California, irrigated. Low rainfall, circumneutral pH.McBride et al., 1999 4.0 Eastern U.S. moderate rainfall, pH 7–7.3.Nguyen, 1998 12.5 High rainfall, pH 5.5–6.9.Hornick et al., 1977 1.8 Eastern U.S. moderate rainfall, circumneutral pH.Average k 5.0

† Calculated assuming that alfalfa uptake of molybdenum is proportional to soil concentration of molybdenum.

isotopes of Mo (Georgievskii et al., 1981). Molybdenum pretreatment program. The concentration of Mo in bio-solids in many regions of the USA began to decreaseis rapidly absorbed, but very rapidly excreted, mainly

in the urine and in part through the bile. High Mo quickly to the 20 mg Mo kg�1 mean (and 75% tile) con-centrations seen today.forages (11 to 32 mg kg�1 ) grown on soils containing

reclaimed mine tailings in Canada had little effect onCu status of grazing cattle, suggesting low bioavailability RISK ASSESSMENTof Mo (Gardner et al., 1996).

Molybdenum-Induced Copper DeficiencyRates of Mo absorption, retention, and excretion areinversely related to the level of dietary S. In sheep, for The limiting risk assessment pathways pertinent toinstance, increasing the dietary S from 1 to 3 g kg�1 in Mo issues associated with land application of biosolidsa diet supplemented with 10 mg Mo per day decreased is Pathway 6 (biosolids → soil → plants → animals).the Mo retention from 37 to 4%. A working hypothesis The original USEPA assessment of molybdenosis riskfor the effect of S on Mo retention is that sulfate inhibits calculated the allowable, long-term biosolids Mo con-membrane transport of molybdate, thus decreasing ab- centration in soil from the algorithm (USEPA, 1992):sorption of Mo in the intestine and decreasing reabsorp-

RPc � RF/UCtion of Mo by the renal tubules (Dick, 1956; Ryan etal., 1987). For sheep with a Mo intake of 0.3 mg d�1, where RPc � cumulative biosolids application limit (kgtotal body Mo decreased from 92.9 to 16.8 mg when Mo ha�1 ); UC � linear uptake slope of forage [(mgsulfate was increased from 0.9 to 6.3 g d�1 (Dick, 1956). Mo kg�1 forage)/(kg Mo ha�1 )] from biosolids-amended

soil; and RF � allowable Mo increment in plant tissueMolybdenum Concentrations in Biosolids (mg Mo kg�1 forage):

In 1988, the USEPA undertook a major effort to char- RF � TPI � BCacterize biosolids chemical composition for use in estab- where TPI � threshold pollutant intake at which a toxiclishing the numerical pollutant limits in the final Part effect is noted in animals consuming the forage (mg Mo503 rule (USEPA, 1990). The National Sewage Sludge kg�1 forage) and BC � background concentration ofSurvey (NSSS) data collection effort began in August pollutant in forage (mg Mo kg�1 forage).1988, and was completed in September 1989. The The initial risk assessment assumed: BC � 2.08 mgUSEPA collected biosolids from 177 wastewater treat- kg�1, TPI � 10 mg kg�1, and UC � 0.423, resulting inment plants and analyzed them for 419 analytes, or RPc � 18 kg ha�1.pollutants, including Mo. Multiple samples were col-lected at some treatment works to characterize the dif- Background Concentration (BC)ferent types of biosolids end products. The NSSS meannational concentration for Mo was 9.24 mg kg�1, with The USEPA selected the BC value of 2.08 mg Mo

kg�1 from the Pierzynski and Jacobs (1986) study, buta standard deviation of 16.6 mg kg�1 (Table 1). Many ofthe detection limit problems (e.g., low percent detected) this represents a very high background concentration

for forages grown in low Mo (uncontaminated) soils.have been attributed to analytical problems (Bastainand Brobst, 1993). Numerous recent literature citations for forages world-

wide (summarized in Kabata-Pendias and Pendias, 1991;Numerous studies (e.g., Logan, 1997) report that con-centrations of most metals in modern biosolids are now Gupta, 1997a; O’Connor and McDowell, 1999) suggest

that a more typical background value for Mo is almostlower than in biosolids sampled for the NSSS. An excep-tion is Mo, the concentration of which increased until always �1 mg kg�1. Plant Mo concentrations vary with

plant species, stage of development, plant part, soil pH,the early 1990s (Logan, 1997). Historical and modernMo data compiled by Brobst (R.B. Brobst, personal soil drainage, soil Mo loads, etc., but uncontaminated

(naturally or anthropogenically), well-drained, non-communication, 2000) suggest an effect of national regu-lations on biosolids Mo concentrations. Sales of molyb- peat-like soils (normal organic matter contents) rarely

support plants with Mo concentrations �1 mg kg�1,dates decreased �25% following promulgation of Part503 in 1993 as publicly owned treatment plants (POTWs) and frequently result in Mo concentrations �1 mg kg�1.

Legumes (e.g., alfalfa [Medicago sativa L.], clover [Tri-attempted to reduce biosolids Mo concentrations tomeet the proposed Table 3 pollutant concentration folium pratense L.], soybean [Glycine max (L.) Merr],

etc.) can accumulate much greater concentrations (2value of 18 mg kg�1. Control of Mo discharges to sani-tary sewers is achieved through local limits in the POTW to 40 mg Mo kg�1 ) under natural conditions, but the


literature (e.g., Miltimore and Mason, 1971, and refer- Mo without reasonable and practical considerations ofCu and sulfate inputs in forage grown on biosolids-ences cited therein) suggests wide variations in legume

forage Mo contents, many �1 mg kg�1, for areas as amended soil and from normal mineral supplementsprovided to grazing livestock seems unnecessarily re-diverse as British Columbia and Nevada. High soil pHs

and elevated natural soil Mo concentrations, or high strictive. Ward (1994) concluded that it was nearly im-possible to identify the equivalent of a NOAEL for Mo,organic matter (peat), poorly drained soils that accumu-

late Mo from leaching (Kubota et al., 1961) typically as the interactions surrounding Mo toxicity are too greatto establish the lower limit. He summarized numeroussupport vegetation with �1 mg Mo kg�1. Such soils have

been mapped for the USA (Kabota, 1977), or are known data sets to conclude that 100 mg Mo kg�1 is definitelytoxic (molybdenosis, e.g., rapid scouring) to cattle, 25historically to produce high-Mo crops and to require

Cu supplementation of grazing animals (Allaway, 1977). to 50 mg kg�1 gives mixed results (sometimes no effect),and that the Mo effects attributed to feeds with �25 mgSuch soils are not likely candidates for additional Mo

input via biosolids, unless special precautions are taken Mo kg�1 are often associated with very low, and poorlyavailable, Cu. We conclude that using the higher endto address Mo issues. For most soils, we believe thatof the NRC critical range (10 mg Mo kg�1 ) as the TPIBC can be realistically and conservatively estimated asis justified.1 mg Mo kg�1, and that the USEPA should adopt the

The TPI is derived for domestic animals, as there arelower value.few data for wild (nondomesticated) animals. Mule deerreportedly tolerate up to 1000 mg Mo kg�1 in their dietsThreshold Pollutant Intake (TPI)(Ward and Nagy, 1977). Flynn et al. (1977) hypothesized

The threshold pollutant intake (TPI) value used ini- a possible Cu � Mo � S interaction to explain abnormaltially by the USEPA was based on guidance from Na- hoof material in moose, but acknowledged that theirtional Research Council (1980), and was taken as 10 mg overall data were consistent with the conclusions ofMo kg�1 animal diet. Ruminants are by far the most Kubota (1974) and others that “available informationsusceptible herbivore to Mo-induced Cu deficiency, and does not suggest an existence of nutritional problemscattle are the most sensitive ruminants (Ward, 1994; in moose due to imbalances of Mo and Cu in feedSuttle, 1991). Most references (Ward, 1994; Suttle, 1991; plants.” Domestic cattle may not be the most sensitiveMcDowell, 1997; Gupta, 1997a) report TPI values that animal to Mo toxicity, but there are no data to justifyrange from a few (2 to 5) to tens (10 to 50) of mg kg�1, selecting another species for use in the risk assessment.and stress the importance of other issues (e.g., forage Further, large, nondomesticated ruminant species typi-Cu to Mo ratios, forage S content, age and condition cally graze large areas, and could be expected to receive

much less biosolids Mo exposure than domestic speciesof the forage, degree of mineral supplementation of theconfined to biosolids-amended pastures.animals, etc.) as significant complicating factors. Unfor-

tunately, attempts to predict Cu–Mo–S–other elementalHighly Exposed Individualinteractions under field conditions have been largely

unsuccessful (Suttle, 1991). The risk assessment in Pathway 6 seeks to protect aThe expert committee report of the National Acad- highly exposed individual (HEI), defined as “the most

emy of Sciences (National Research Council, 1980) eval- sensitive/most exposed herbivorous livestock that con-uated low-level, chronic Mo toxicity, and identified “5 sumes plants grown on biosolids-amended soil. It is as-to 10 mg Mo kg�1, which has been weakly associated sumed that 100% of the livestock diet consists of foragewith impaired bone development in young horses and grown on sewage sludge–amended land, and that thecattle” as the critical level. However, substantially animal is exposed to a background pollutant intake”higher levels of Mo are tolerated in the presence of ade- (USEPA, 1994). Grazing ruminants may, indeed, bequate Cu and inorganic sulfate. Forages grown on bio- limited to forage growing on biosolids-amended land,solids-amended soils (high cumulative biosolids loads) but dietary intake of common mineral supplements con-are typically normal (nondeficient) in Cu and sulfate, taining Cu (that can obviate low Cu to Mo ratios of

forage) is ignored in the risk assessment. Further, con-so the higher permissible Mo concentration recommen-fined ruminants (finishing beef cattle or dairy cows) aredation of 10 mg Mo kg�1 seems appropriate. A largeusually fed a variety of forages, grains, and mineralbody of data on the toxicity of Mo in forages grown onsupplements to maximize performance. How reasonablesoils naturally high in Mo (not Mo salt additions tois it to assume that 100% of the ruminant diet is oneanimal diets) supports the use of 10 mg Mo kg�1 forkind of forage grown exclusively on biosolids-amendedforages with normal Cu concentrations in the diet (Na-land? What mitigating effects do supplemental Cu andtional Research Council, 1980 [Table 1]; Suttle, 1991).possible increased forage Cu (as a result of biosolids)The TPI used by the USEPA represents the best avail-to the diet have on the risk of Mo-induced hypocu-able data for domestic animals, and may be consideredprosis? We examine the diet assumptions used to assessa lowest observed effect level (LOEL) rather than a noMo toxicity risk to ruminant livestock below.observed adverse effect level (NOAEL). This distinction

is important, as other pathway analyses in Part 503 reliedDietary Assumptionson NOAEL values (when available) to build conserva-

tism into the risk assessment. Given the complexity of Those livestock classified as ruminants include cattle,sheep, and goats. Given the greater sensitivity of cattleCu–Mo–S interactions, however, focusing exclusively on


to Mo-induced hypocuprosis, we focus on cattle. Cattle and slaughtered after about 120 d on feed, they are notcan be separated into beef and dairy because of the dif- considered at risk for Mo-induced hypocuprosis. Beefferences in their feeding management. Risk assessment cattle are fed conserved roughages (hays, silages, andfor sheep and goats can be considered similar to either crop aftermath) during the nongrazing seasons. Duringdairy or beef cattle, depending upon their relative feed- the growing season, pastures for beef cows are domi-ing management. nated by grasses, although variations exist among re-

Dairy Cattle. Feeding management of dairy cattle can gions in the USA. Legumes (alfalfa and clovers) arebe divided into calves (0 to 3 mo), young heifers (3 to often incorporated into pastures, but they rarely consti-6 mo), growing heifers (6 mo to breeding), pregnant tute the entire ration of beef cows for extended periods.heifers (15 to 20 mo), lactating cows (305 d), and nonlac- Mixed plant species in a pasture assist in lengtheningtating cows (60 d). Calves typically are born with high the grazing periods and allow for plants that are bestconcentrations of Cu (�300 mg Cu kg�1 of dry matter) in suited to the soil conditions within a pasture (Etgen ettheir liver (Underwood, 1981) and these concentrations al., 1987). Young beef calves consume some fresh for-decline over several months to those typical of adult age, and the amounts progressively increase as the calfruminants (Kincaid et al., 1986). Concentrates comprise grows and the milk production of the dam declines.most of the dry feed for calves and young heifers; thus, Weaned beef calves (age � 259 d) may be fed onlyMo-induced hypocuprosis is unlikely to occur in calves roughage until they enter the feedlot for fattening. Theand heifers because of the endogenous Cu reserves, use diets of these weaned calves (stockers) can include cropof concentrates containing Cu supplements, and restricted residues (corn stalks, cereal grain straws, and stubble),intakes of fresh forages in diets of these animals. Grow- winter wheat (Triticum aestivum L.) (or other smalling heifers (6 mo to breeding) are typically fed concen- grain) pastures, irrigated pastures, silages, and hay (Ens-trates along with their forage. Once heifers are pregnant, minger et al., 1990).they are usually fed only forage and mineral supplements The cattle groups perhaps at greatest risk of Mo-until 2 to 4 weeks prepartum. Lactating dairy cows are induced Cu deficiency are beef cows, growing beeffed diets containing between 40 and 60% forage, and 60 calves, and pregnant heifers because of the dominanceto 40% concentrates (Ensminger et al., 1990). Concen- of fresh forages in their diets. Attention to the concen-trates for lactating cows consist of about 50% grain (e.g., trations of Mo, Cu, and S in their diets is needed andcorn [Zea mays L.] or barley [Hordeum vulgare L.]), 20% especially to the trace mineral supplementation pro-by-product feeds (e.g., whole cottonseeds, beet pulp, and grams provided for these animals when Mo problemswheat mill run), and 20% protein supplement (e.g., soy- are expected.bean meal), with the remainder (10%) being molasses, The risk of Mo-induced Cu deficiency is greatest dur-sodium bicarbonate, mineral supplements, vitamin sup- ing the period of active growing forage, which is only 5plements, and various other ingredients. to 6 months in many areas of the country. Molybdenum-

The forage portion of dairy cow diets varies among induced Cu deficiency is not a problem for ruminantsregions of the country (Mowrey and Spain, 1999). Often, receiving stored forages, apparently because of in-the forage consists of near equal proportions (dry matter creased availability of Cu and reduced availability ofbasis) of hay and silage during the nongrazing seasons, Mo in these feeds (Underwood and Suttle, 1999). Mostto as much as 100% fresh forage during the 4- to 6-month

important, Mo-induced Cu deficiency regions in thegrazing season. The fresh forage can consist entirely ofUSA are well known and farmers have learned to com-grasses and legumes, although mixed pastures are mostpensate by providing Cu in mineral supplements (Alla-common (Etgen et al., 1987). Regardless of the pastureway, 1977).forage species, the entire ration of the dairy cow rarely

The use of a single TPI value of 10 mg Mo kg�1 is anconsists of more than 60% fresh legumes because of theoversimplification of general animal response to forageneed to incorporate other feed ingredients into diets toMo exposure. Nevertheless, we believe that the TPImaximize milk production. Most large herds of dairyvalue chosen is reasonable for a national risk assessmentcattle in the USA do not graze pastures, and their dietsfor biosolids Mo when practical aspects of animal (HEI)remain fairly constant during all seasons of the year.management (e.g., mineral supplementation and totalNonlactating (dry) dairy cows are fed roughages untilanimal diet considerations) are recognized.14 d prepartum, when limited amounts of concentrates

are introduced into the diet to prepare the cows for thelactation ration fed after parturition. Nonlactating dairy Allowable Molybdenum Increment (RF)cattle normally consume forages consisting of grasses or

Based on the above discussion, the allowable Mo in-legume–grass mixes, but are not fed 100% fresh legumescrement in plant tissue (RF) is:because of possible health problems associated with ex-

cessive intakes of protein, energy, potassium, calcium, RF � TPI � BCand increased incidence of bloat (Etgen et al., 1987;

� 10 � 1Ensminger et al., 1990). During the nonlactating period,cows are provided mineral supplements. RF � 9 mg Mo kg�1

Beef Cattle. Beef cattle production can be dividedTo complete the risk assessment using the USEPA’sinto the cow–calf operation, stockers, and feedlot cattle.

Because feedlot cattle are fed high-concentrate diets original algorithm, RF is divided by UC to arrive at RPc.


Uptake Coefficient (UC) contribution of deeper soil profile Mo to plant uptake.Thus, even if surface soil sampling occurs each year ofProblems associated with appropriate selection and/a multiyear study, soil Mo accessible to deep-rootedor calculation of UC values are many. Analytical prob-plants may be underestimated. Another shortcoming oflems with Mo (e.g., falsely high Mo analysis due to Femany studies is the minimal range or number of soiland Al interference and high limits of detection withMo loadings studied. Under these conditions, single-some methods; McBride et al., 2000) probably confoundpoint estimates of UC must be made. This is done byinterpretation of even some modern literature. Further,subtracting the Mo concentration found in the controlmany plant Mo uptake studies were conducted in the(no added Mo) plants from the concentration in plantsgreenhouse, and probably suffered greenhouse effect er-grown on the biosolids-amended soil, and then dividingrors (higher uptake slopes for contaminants comparedby the biosolids Mo load.with those found in the field at similar contaminant

loads) discussed in the Part 503 Technical Support Doc-Variations in Uptake Coefficient with Timeument (USEPA, 1992).and Plant PartIdeally, the UC value is obtained from field experi-

ments where ranges of soil Mo loadings are evaluated. Using point estimates of UC values is appropriateIn this case, UC is calculated as the slope of the linear for whole plant estimates of Mo exposure when, forregression of plant tissue Mo concentrations (mg kg�1 ) example, corn silage is fed, but not when perennial for-versus biosolids Mo application (kg ha�1 ). The approach ages are consumed. In such cases, UC values changeimplies that the plant tissue Mo response to soil Mo monthly (and widely) over an entire grazing season (e.g.,load is linear and that the applied Mo remains in the Ferguson et al., 1943; Nguyen, 1998), with plant partroot zone indefinitely. The linear model was assumed actually consumed (grains vs. stover, e.g., Gupta, 1997b),by the USEPA in the initial risk assessment for all metal and with forage condition (fresh vs. dried hay, e.g., Millsuptake calculations, but data in the Part 503 Technical and Davis, 1987). O’Connor and McDowell (1999) rec-Support Document, and more recent data (e.g., Barbar- ommended calculating (yield) weighted average Moick et al., 1995) suggest a plateau model as more appro- concentrations of grass grazed for 6 mo by cattle. Thepriate for at least some metals or crops. Limited data weighted average concentration was thought to morepresented by O’Connor and McDowell (1999) and Ngu- accurately represent the forage Mo concentration theyen (1998) suggest that the plateau model may also be cattle experienced throughout the growing season thanappropriate for biosolids Mo applied to a pasture grass. simply calculating the average concentration of severalUsing a linear model when a plateau model is appro- cuttings. The weighted average Mo concentration waspriate overestimates crop Mo (and risk) at higher bio- also thought to more reasonably represent the animalsolids application rates and over extended periods of forage consumption (Mo exposure) that varied withapplication. Given the incompleteness of the database, grass yield throughout the grazing season.a linear model is assumed herein.

Variations among Plant SpeciesSoil Molybdenum Load

Variations in plant species Mo concentrations—at theObtaining the plant Mo concentrations for the UC same soil Mo load—are widely acknowledged (e.g.,

calculations is relatively straightforward, but determin- Gupta, 1997b; Vlek and Lindsay, 1977; Kabata-Pendiasing the soil Mo loading is less so. The most desirable and Pendias, 1991; Johansen et al., 1997) and, in fact,situation is to have measured total soil Mo concentra- form the basis for management of cattle Mo intake ontions from a sampling time close to when the plants were (known) high-Mo areas. Ranchers are advised to plantgrown. These concentrations can then be converted to nonaccumulating grasses or grains, rather than accumu-soil Mo loadings (applied from biosolids) by multiplying lators such as legumes (e.g., alfalfa, clover, and soybean).by the appropriate factor, considering sampling depth Miltimore and Mason (1971), however, cite several dataand bulk density, and the background Mo concentration sets that show little difference in Mo concentrations inin similar nonamended soil. For a sampling depth of 15 grass, grass–legume, legume, or corn silage cattle dietscm and a bulk density of approximately 1.3 Mg m�3, grown in areas as diverse as British Columbia, Canada,one multiplies soil concentration by two to obtain soil Kansas, Virginia, and Nevada. Soil pH, wetness, MoMo loading in kg ha�1. This approach is consistent with concentration, and climate can all apparently play morethe assumption in the risk assessment that Mo is not a important roles in determining forage Mo concentrationconservative element in the soil. That is, if some time than forage species alone. Nevertheless, legumes arehas passed since the biosolids Mo was applied, leaching particularly susceptible to excessive Mo accumulationmay have reduced the soil Mo concentration to levels (high uptake slopes), and databases used to assess Molower than those predicted from the original Mo loading toxicity should include legume UC values.rate (biosolids rate � biosolids Mo concentration). Un-fortunately, few published studies report total soil Mo

Variations with Soil Propertiesconcentrations for each of multiple cropping seasons,and the original Mo loading rate must be used in the UC Variations in plant-available Mo with soil pH are

well known (e.g., Gupta, 1997a,b; Kabata-Pendias andcalculation. In most studies, soil sampling and analysis isrestricted to the 0- to 15-cm depth, and ignores possible Pendias, 1991; Pierzynski and Jacobs, 1986; Williams


and Gogna, 1981). High soil pH favors low Mo sorption viously mentioned, total soil Mo concentrations thatcould be used to calculate Mo loadings would be prefer-and high plant availability. Molybdenum adsorption en-

velopes typically exhibit maximal Mo sorption at soil able to calculated Mo loadings based on biosolids com-position and application rates. Few studies satisfy allpH values �5, so near-neutral and calcareous soils tend

to retain little Mo (e.g., Goldberg et al., 1996, 1998). these criteria, and the selection of appropriate data setsfrequently requires use of professional judgement. OneMost molybdenosis problems occur on such high-pH

soils (Allaway, 1977). essential requirement is that the UC values be generatedfrom studies in which biosolids were the Mo source.Variations in soil moisture and soil organic matter

contents affect plant Mo concentrations. Kubota et al. Data from greenhouse pot studies would only be used ifno other data were available for a particular forage type.(1963) showed that the same soil Mo concentration re-

sulted in vastly different plant Mo concentrations, de- The USEPA attempted to resolve the UC value varia-tion issues by calculating a geometric mean of UC esti-pending upon the soil moisture regime. Ready supply

of Mo in moist (poorly drained) soils is well recognized mates from a limited set of field- and greenhouse-gener-ated data, where biosolids were the sources of Mo load.(Kubota, 1977), and is one reason given for the abundant

Mo in plants growing in wet, high-organic soils (e.g., The original Mo data set used in the 1993 rule devel-opment was quite limited, but a few significant studiespeats) even at relatively low soil Mo concentrations

(Allaway, 1977). In “normal” soils (well-drained, �50 g (Basta et al., 1999; O’Connor and McDowell, 1999; Mc-Bride et al., 2000; O’Connor et al., 2001a) that meetkg�1 soil organic matter), pH is usually the dominant

factor determining Mo phytoavailability. Soils with pH most of the criteria described above are now available.The data are included in Table 2, along with selectedvalues �6 frequently result in forage with excessive

(10 to 20 mg kg�1 ) Mo concentrations if soil Mo concen- data from Tables C-39, C-40, and C-41 of the TechnicalSupport Document (USEPA, 1992). Still underrepre-trations are significantly above background levels (1sented in the table are data from field studies whereto 2 mg Mo kg�1 ) (Gupta, 1997a; Kabata-Pendias andlegumes are grown in biosolids-amended soils of highPendias, 1991; Barber, 1984; Allaway, 1977).pH, and where the biosolids have less than the ceilingMo concentration. A paper (O’Connor et al., 2001b)Biosolids Source Effectsdescribing one such set of soybean grain data has been

Biosolids source effects, based on excessively high published; data are included in Table 2.total biosolids Mo concentrations (e.g., Pierzynski and Uptake coefficients (UC values) of nonlegumes areJacobs, 1986), or other constituents (Fe and Al) in the low and almost always �0.5 (Table 2). The lone excep-biosolids (e.g., Soon and Bates, 1985; O’Connor and tion (UC � 4.6) in the database comes from a studyMcDowell, 1999) can also lead to vastly different UC involving a pasture grass grown in soil amended withestimates. Such a biosolids effect was not directly con- one biosolids that was inadvertently overlimed in thesidered in the original USEPA risk assessment, although second year of a 2-yr study (Nguyen, 1998). Anotherthe Technical Support Document (USEPA, 1992) in- biosolids (slightly higher Fe and Al content) applied tocludes reference to data of Soon and Bates (1985) show- the same soil yielded a more representative UC valueing lower Mo phytoavailability on soil amended with Fe for the grass of 0.39. The arithmetic average of the UCor Al biosolids compared with Ca biosolids amendment. values for 29 nonlegume entries in Table 2 is 0.24. WeFerric chloride and/or alum are routinely added in waste conclude that a UC value for nonlegumes (vegetationtreatment processes to improve P removal, and would or grain) is conservatively estimated as 0.5.be expected to be similarly effective at immobilizing Mo. Field data for estimating UC values for legumes areLime-stabilized biosolids can raise soil pH and increase limited, so greenhouse data (Pierzynski and Jacobs,uptake slopes correspondingly (Soon and Bates, 1985; 1986; McBride et al., 2000) are included in the databaseMcBride, 1998). (Table 2). The arithmetic average of UC values for 24

The original USEPA risk assessment included the legume entries is 2.2. Given the limited diversity ofvery high (1500 mg Mo kg�1 ) biosolids data of Pierzyn- studies, we conclude that a UC value for legumes isski and Jacobs (1986), but data for such a biosolids (Mo conservatively estimated as 4.0. No adjustment of theconcentration 20-fold greater than the 98th percentile UC value is made for the well-recognized decreased Moof national biosolids) represent unique conditions. We availability to cattle in dried (vs. fresh) forages (Millsbelieve that the USEPA should omit the Pierzynski and and Davis, 1987).

Based on the dietary considerations presented pre-Jacobs (1986)-derived UC values when better data areavailable. viously, we estimate that grazed fresh legumes will typi-

cally constitute no more than 50% of beef cattle or dairyThe ideal data set for purposes of risk assessmentwould be from field studies in which Mo was added at cow animal diets, and frequently less. The remainder of

the diets would typically consist of hay silage, roughagevarious rates from biosolids containing less than 75 mgMo kg�1 (maximum biosolids Mo concentration allowed (grain by-products), and grains, plus mineral supple-

ments. If an average UC value for fresh legumes is takenfor land application). In addition, having UC values forall types of forages typically consumed by animals in conservatively as 4, and an average UC value for all

other plant-feedstuffs is taken very conservatively asthe exposure pathway of concern would be desirable.Data for corn silage, stover, or grain would be preferable 0.5, a diet-weighted UC value of [4(0.5)] � [0.5(0.5)] �

2.25 is obtained. We believe that such an UC valueto corn leaf diagnostic tissue data, for example. As pre-


represents a worst-case estimate of typical forage Mo Brobst, personal communication, 2000) conductedan informal survey of contemporary biosolids use inexposure, and note that it ignores normal mineral (Cu)

supplementation recommended for good animal man- 15 states, from Georgia to Oregon and from Minne-sota to Arizona. Twelve of the states applied �1% ofagement.their biosolids to pastures; Oklahoma and Georgia ap-plied �10%, and Virginia applied �33%. AgriculturalAlgorithm Modificationsproducers tended to use the nutrients in biosolids on

Fraction of Diet Affected (FC) croplands (rather than pastures) whenever possible toreduce production costs associated with commercialNot all feed consumed by cattle is grown in the samefertilizers.place, nor is all the land used to grow animal feed likely

The land application weighting factor (Column I) esti-to be biosolids-amended. It is particularly unlikely thatmates the possible increases in biosolids production andthe feed-producing land would be amended every yearthe resulting fraction of land affected by land applica-for a total application rate of 1000 Mg ha�1 (10 Mg ha�1

tion. Column I values were derived by multiplying theyr�1 � 100 yr), as was assumed in the risk assessmentpercent of biosolids currently land-applied by 1.5, up to(USEPA, 1992). More likely, the feed-producing landa maximum of 100% of the biosolids produced. Columnwould be amended at 5 to 10 Mg ha�1 (N-based applica-J is the product of Column H and Column I, and repre-tion rates) only periodically (e.g., once every 3 to 5 yr).sents a conservative estimate of pasture land (cattleWe examined biosolids production and use on crop andfeed) likely to be affected by biosolids (FC). Twenty-pasture land in each state to estimate the fraction offour states have FC values �1%, 15 have values betweencattle diet (FC) likely to be affected by biosolids use.1 and 10%, 5 between 10 and 20%, and 6 have FCBiosolids production is likely to remain the same orvalues �20%. None of the six states (Pennsylvania, Newincrease only slightly over the next several years. Waste-Jersey, Connecticut, Delaware, Maryland, and Massa-water treatment plant construction has slowed, andchusetts) was among the top 28 beef-producing statesincreases in biosolids production are related to improve-in 1997 (USDA, 1999). We conclude that a reasonablements in existing treatment rather than new construc-estimate of the fraction of ruminant forage likely to betion (Bastain, 1997). Estimates of biosolids productionaffected by biosolids (FC) is 0.1 to 0.2, and recommendand final use and disposal were surveyed in 1996; theusing the more conservative value of FC � 0.2 for atotals for the USA at that time were 6.8 � 106 dry Mgnational approach to rule making. The FC factor weproduced, with 54% of the total being land-applied (Bas-propose may not be universally applicable, but is consis-tain, 1997). Table 3 contains a summary of the quanti-tent with USEPA policy that estimates the fraction ofties of biosolids produced and land-applied in each state.

Column B (Table 3) represents total acreage in farms HEI diet probably affected by food grown on biosolids-and ranches held as private lands in 1997 (USDA, 1999). amended land in Pathways 1, 2, 4, and 5 (USEPA, 1992).Column C represents land in crop rotation that, during Local conditions may warrant using a different FC,the year of the survey, was in pasture for at least part which would allow site-specific considerations in a bio-of the year. Reviews of past USDA agricultural surveys solids land application program.suggest that acreages in this category differ little fromyear to year. Pasture and rangeland acreage (Column Leaching Correction (LC)D) represents lands remaining in pasture for several

Maximum Mo loading considerations ignore the factyears; generally considered permanent pasture. Pastthat Mo is not a conserved element when biosolids areUSDA agricultural surveys (back to 1987) suggest simi-applied to the same field for many years, especially tolar acreages. Column E values are the total acreages insoils having high soil pH where Mo leaching, bioavail-pasture (Columns C � D), but do not include grazingability, and risk are all maximized. Few studies havelands leased from government agencies. Addition ofbeen conducted with the primary objective of directlythese public lands would significantly increase the acre-characterizing Mo leaching dynamics and the parame-age, particularly in the 11 western states. Data for bio-ters affecting leaching rates. Nonetheless, several stud-solids produced in each state (Column F) were summa-ies provide indirect evidence of Mo leaching from bio-rized by Bastain (1997). The values do not account forsolids and industrial Mo sources. These studies areintrastate transfer of biosolids, such as occurs from areassummarized below, and demonstrate that Mo leachingwith small land bases to areas with large land bases.from the plow layer occurs, sometimes at high rates. Ad-A biosolids load of 5 Mg ha�1 was chosen as a typicalditional studies of Mo leaching from biosolids sourcesapplication rate to pasture land, and was used to cal-are recommended to develop a more complete data setculate the acreage required to accommodate the loadand to validate the approach used here.(Column G).

Molybdenum is adsorbed by acidic soils, and exhibitsColumn H represents land required for biosolids ap-maximal retention at soil pH values �5 (Goldberg et al.,plication (Column G) as a percentage of total land in1996, 1998). O’Connor and McDowell (1999) presentedpasture (Column E). The calculation included all bio-data for Mo sorption on biosolids-amended soils thatsolids produced in each state, regardless of use and/orconfirm Mo behavior noted by Goldberg for unamendeddisposal practice (e.g., land-applied, landfilled, or in-soils. Their data also confirm the dramatic reduction incinerated), and all biosolids were assumed to be applied

to pastures, a conservative assumption. Brobst (R.B. Mo retention as soil pH increases, with sorption becom-


ing negligible above pH 6. Thus, Mo availability to plants concentrations at �25 cm. They were unable to accountfor all of the Mo added, and hypothesized Mo leaching.(and to leaching) increases dramatically at higher pH.

Artiola (J.F. Artiola, personal communication, 1999) Nguyen (1998) noted about 50% loss of biosolids Mofrom the surface 0- to 15-cm depth of a limed acid (pHconducted column studies with calcareous soils (pH �

7.8) amended with biosolids Mo. The biosolids applica- 5.5–6.9) Spodosol 3 to 4 yr after biosolids application.Thus, even slightly acid soils under high-rainfall condi-tion rate was about 200 Mg ha�1, and the New York

biosolids Mo concentration was 6 g Mg�1 (Mo load � tions can be expected to allow leaching of biosolids Mo.Leaching would be promoted if the soils were limed1.2 kg Mo ha�1 ). Molybdenum moved through the col-

umns essentially unimpeded, and reached low relative or amended with high-pH (alkaline-treated) biosolids(McBride, 1998).concentrations (C/Ci � 0.1) in drainage after only about

two pore volumes of drainage. There was little differ- Leaching of Mo under nonirrigated, semiarid, or aridconditions is often difficult to predict. Infiltration belowence in Mo leaching behavior whether the Mo was

added as biosolids or Mo salts under such high-pH (7.8) the root zone occurs when the magnitude and durationof moisture events (e.g., snow melt, rainfall) exceed evapo-conditions. O’Connor and McDowell (1999) and Brin-

ton and O’Connor (2000) reported data that suggested transpiration, runoff, soil moisture retention, and ab-sorption by surface materials (e.g., biosolids). McCurrydifferent effects of biosolids source on Mo retention

and/or release depending upon biosolids total Fe and (1995) summarized infiltration data collected in severalstates. Data represented infiltration studies on biosolidsAl contents, but soil pH effects dominated Mo behavior

in two soils amended with the various biosolids. High projects in Colorado and New Mexico and basic infiltra-tion studies conducted in New Mexico, Idaho, Califor-soil pH reduces soil retardation of Mo movement and

increases the likelihood that applied Mo will leach away nia, Texas, Oklahoma, and Utah. Infiltration data fromthe biosolids studies were consistent with data collectedfrom the zone of biosolids incorporation. The effect

would be greatest under irrigated conditions, where net for nonbiosolids studies. Moisture infiltrated 40 to�270 cm depending upon location and type of excessdownward flow of water is maintained (positive leaching

fraction) to control salinity. Chang and Page (2000) re- moisture event (McCurry, 1995). Excess moisture inarid and semiarid regions is usually only available incently conducted an input–output balance of trace ele-

ments in soils of the San Joaquin Valley’s West Side. the spring and early summer, following snow melt, and/or for briefs periods following intense summer thunder-Numerous inputs were considered, including Mo from

biosolids additions. Despite the inputs from various storms. McCurry’s data demonstrate that water (anddissolved ions) can move below the root zone duringsources, there was a net depletion of Mo from cropland

on the West Side (Chang and Page, 2000). Amounts of these periods. Additional measurements of solute move-ment through biosolids-amended soils under semiaridMo dissolved from soils and transported to tile drains

exceeded amounts of Mo added from all input sources and arid conditions have been made (Janonis et al.,1996; Michalk, 1995; Moffet et al., 1995). Molybdenumcombined. Leaching of Mo from these near-neutral soils

accounts for the net depletion of Mo, and is inevitable was not specifically monitored in either study, but isexpected to move as readily as other anions (e.g., PO4,for sustainable irrigated crop production (Chang and

Page, 2000). and SO4 ) whose migration was detected. Thus, leachingof Mo can be expected in all but the driest of environ-Phillips and Meyer (1993) studied alfalfa growing in

calcareous (soil pH � 7) fields with natively high soil Mo ments, and can be expected to be significant underirrigated or high-rainfall conditions. Under dryland con-concentrations in Kern County, CA. An earlier (1950)

survey of alfalfa from the county had identified average ditions, salt accumulation typically limits biosolids ap-plication rather than N, P, or Mo loads.alfalfa tissue Mo concentrations of about 10 mg kg�1.

Resampling the same fields 35 yr later revealed average Leaching loss of Mo is expected to be greatest underhigh soil pH conditions, where Mo bioavailability isalfalfa tissue Mo concentrations of about 3.5 mg kg�1.

No quantification of soil Mo concentrations was at- problematic. Not accounting for Mo losses to leaching,even over the long periods (�100 yr) needed to attaintempted, but Phillips and Meyer concluded that the

lowered tissue Mo concentrations were associated pri- limiting cumulative soil Mo loads, is unrealistic.Pollutant leaching can be characterized using rigorousmarily with leaching of soluble salts (including Mo).

Similarly, McBride et al. (1999) reported that nearly quantitative approaches or more qualitative approaches.The USEPA, for example, used two transport models80% of biosolids Mo applied at high rates to a calcareous

silty clay loam (pH 7.0 to 7.3) had been lost from the (quantitative approach) to predict ground water effectsof land-applied biosolids-pollutants in the Pathway 12topsoil under natural rainfall conditions over the nearly

20 yr since the biosolids were applied. and 14 (drinking water) risk assessment. The VADOFsubroutine of the RUSTIC model (USEPA, 1989) wasLeaching of Mo is not restricted to high-pH soils.

Hemkes et al. (1980) applied moderate rates (6 to 18 Mg used to estimate flow and pollutant transport throughthe unsaturated zone. A second model (AT123D; Yeh,ha�1 ) of high-Mo biosolids (117 to 170 g Mo Mg�1 ) to

a pH 5.9 sandy, permanent pasture soil in the Nether- 1981) was then used to estimate transport in the satu-rated zone (aquifer). The combined model outputs esti-lands each year for 3 yr (total Mo loads � 2.1 to 9.2 kg

Mo ha�1 ). Molybdenum concentrations in the surface mated pollutant transport to a receptor, a drinking watersupply well. Results of the simulations were used to(0–2.5 cm) soil reached 7.4 mg kg�1 at the greatest bio-

solids Mo load, and decreased with depth to background back-calculate reference pollutant application rates that


result in threshold ground water effects at the receptor rather, most reported changes in soil Mo concentrationsmany years after initial Mo contamination. The field(USEPA, 1994). This rigorously quantitative approach

is data- and assumption-intensive, and is deemed inap- data are presented in Table 4, and do not include thedetailed laboratory data of Artiola (J.F. Artiola, per-propriate for Pathway 6 risk assessment for two reasons.

First, the receptor of interest in Pathway 6 (the most sonal communication, 1999), which suggest very highsensitive pathway of risk for Mo) is a ruminant grazing biosolids Mo leaching rates under uniform, short-termbiosolids-amended forage, not a human drinking water leaching conditions. Data in Table 4 represent estimatedfrom a downstream well. Second, model parameters annual Mo leaching rates of biosolids Mo (McBride etwere set to maximize pollutant leaching in Pathways 12 al., 1999; Nguyen, 1998) and natural (Phillips and Meyer,and 14 (USEPA, 1992), so risk in Pathway 6 is simultane- 1993) or anthropogenic (Hornick et al., 1977) Moously underestimated (less Mo remaining in the soil for sources. The data represent leaching periods of 3 to 35plant uptake). For these reasons, we chose a simplified, yr. The average leaching rate (k) for data in Table 4 isbut conservative, model that uses a first-order leaching about 5% yr�1, with a range of 1.8 to 12.5% yr�1. Thealgorithm and empirical data for pollutant leaching USEPA (1992) used a leaching rate of 12% yr�1 for As,characterization. The algorithm describes leaching that an anion expected to exhibit soil mobility similar to Mo.annually removes Mo from the root zone in proportion Net soil Mo load (kg Mo ha�1 ) is calculated as ato the total Mo concentration in the soil (Eq. [1]): function of time, assuming an application of 10 Mg ha�1

yr�1 of biosolids containing 40 and 75 mg Mo kg�1 atdCy/dt � �kCy [1]1.8% yr�1 leaching (Fig. 1) and 5% yr�1 leaching (Fig.

where Cy is the Mo concentration (load) in soil (mg 2). Figure 1 predicts that a biosolids containing 40 mgha�1 ) for any year, t is time (yr), and k is the leaching Mo kg�1 can be safely applied for 100 yr without ex-percentage per year (% yr�1 ). The loss of Mo annually ceeding the 20 kg Mo ha�1 diet-weighted (FC-corrected)due to leaching is represented by dCy/dt, and the concen- criterion when the smallest annual leaching rate (k �tration of Mo in soil in any year (Cy ) is calculated as 1.8% yr�1 ) is assumed. Figure 2 predicts that even athe sum of Mo left after leaching the previous year biosolids containing the ceiling concentration of 75 mg(Cy�1 ) and Mo added in the current year (Cadded ); Cy � Mo kg�1 can be applied for 100 yr without exceeding aCy�1 � Cadded. plateau Mo load of 16 kg ha�1 when k � 5% yr�1. A

The model assumes relatively constant climatic condi- biosolids containing 40 mg Mo kg�1 could be appliedtions over, for example, the maximum assumed 100-yr for 100 yr (at 5% leaching yr�1 ) and never exceed 8 kgbiosolids application period. Further, one assumes a Mo ha�1, well below the soil load associated with Mo-constant pollutant addition rate and a constant (aver- induced hypocuprosis, even when the dietary factorage) pollutant leaching rate (k). If no leaching is as- (FC) is ignored. High soil pH exacerbates plant Mosumed (k � 0), Mo accumulates in the soil in direct uptake, but also promotes Mo leaching, so long-termproportion to the addition rate. When k � 0, the model Mo risk is minimized.projects that the quantity of Mo leached will eventually A leaching correction (LC) factor can be derived fromequal the quantity added, resulting in a steady-state the figures by dividing the net soil Mo load remaining(plateau) soil Mo concentration (load). The plateau con-centration depends on the annual Mo addition rate andthe assumed annual Mo leaching rate. The critical condi-tion in the risk assessment for Pathway 6 is that theplateau Mo concentration be less than the soil Mo con-centration associated with forage Mo effect on cattle.

Average (long-term) leaching rates do not character-ize pollutant leaching in the short term. Leaching istypically nonlinear, with high initial rates, followed byprogressively slower rates in subsequent years as pollut-ant mass decreases. We regarded constant linear ratesas appropriate for two reasons. First, biosolids additionsare incremental over the assumed 100-yr site life, whichbetter fits a constant, linear loss per year assumption.If the entire cumulative biosolids load were applied inone year, a nonlinear leaching model would be moreappropriate. Second, selection of an average (long-term) annual loss rate results in less leaching estimationin the short term (when soil Mo concentrations arehigh), which leaves more Mo available for plant uptake.Overall, we believe such assumptions are more protec-tive of the Pathway 6 HEI.

Fig. 1. Net soil Mo load with time when soil is amended with biosolidsWe estimated long-term Mo leaching rates (k values) containing either 75 or 40 mg Mo kg�1 at 10 Mg biosolids ha�1

from various literature sources mentioned previously. yr�1 and the leaching coefficient is either zero (no leaching) or1.8% yr�1.Few published studies quantified annual Mo leaching;


Numerical Standards for Molybdenum

Based on the above considerations and the modifiedalgorithm presented, we suggest the following numericalstandards for Mo in the land application of biosolids:

Ceiling concentration � 75 mg Mo kg�1

Cumulative pollutant loading rate � 40 kg Mo ha�1

Alternate pollutant limit � 40 mg Mo kg�1

Additional ConsiderationsAnimal and Pasture Management

Copper deficiencies in forage are common worldwide(Gartrell, 1981), and copper deficiency significantly af-fects ruminant livestock production in large areas of theworld (McDowell, 1992, 1997). Similarly, Mo-inducedhypocuprosis has been widely recognized as a problemin selected areas of the USA, Canada, Europe, andAustralia for decades, and livestock owners have had

Fig. 2. Net soil Mo load with time when soil is amended with biosolids corrective management practices recommended to themcontaining either 75 or 40 mg Mo kg�1 at 10 Mg biosolids ha�1

for �50 yr (e.g., Lewis, 1943; Cameron and Goss, 1948).yr�1 and the leaching coefficient is either zero (no leaching) or5% yr�1. The best primary management practice is to supplement

cattle feed with added Cu; typically, 10 mg Cu kg�1 ofdiet, but increasing to 25 mg kg�1 during pregnancy,after 100 yr by the total Mo load added. Thus, for aand to as much as 50 mg kg�1 if “animals have access tobiosolids containing 40 mg Mo kg�1 and at 1.8% leachinghigh sulfate water” (Gooneratne et al., 1989). Allawayper year (Fig. 1), the leaching correction factor is:(1977) concluded that “stockmen in the USA have metthe problems of Mo toxicity by treating the animals,LC �

18 kg Mo ha�1 remaining40 kg Mo ha�1 added

� 0.45rather than measures applied to the soil or crop. Thegeneral utility of Cu therapy to prevent Mo toxicity hasand at 5% leaching per year (Fig. 2):minimized efforts to meet the problem through soil orplant management.”LC �

8 kg Mo ha�1 remaining40 kg Mo ha�1 added

� 0.2 Thus, Mo-induced Cu deficiency problems are wellknown, easily recognized, and easily corrected by

We believe that a conservative correction for leaching ranchers operating in areas prone to Mo toxicities.(LC � 0.45) makes the risk assessment appropriately Ranchers and farmers, who know from decades of expe-realistic, but recognize that a different LC value could rience that their soils produce crops prone to Mo accu-be necessary as additional field-scale leaching data be- mulation, are unlikely to intentionally add high Mocome available. loads via biosolids, or any other soil amendment, unless

Incorporating Mo leaching considerations into the this is done in conjunction with Cu supplementation.Pathway 6 algorithm yields the following: Ranchers or dairymen receiving forage from elsewhere

are not likely to feed cattle excessive amounts of Mo-RPc � (RF/UC) � (1/FC) � (1/LC)accumulating plants (e.g., legumes) indiscriminately.

� (9/2.25) � (1/.2) � (1/.45) Imported forage is typically dry hay, which has a muchlower risk of Mo-induced hypocuprosis (e.g., Suttle,� 44 kg Mo ha�1

1983; Mill and Davis, 1987; Underwood and Suttle,Following the USEPA policy of rounding down criti- 1999). Large animal feeding operations typically keep

cal limits, we derive an RPc value of 40 kg Mo ha�1, close watch on animal condition and diet, and wouldand a corresponding alternate pollutant limit (APL) of logically address a potential Mo problem quickly with40 mg Mo kg�1 for Part 503 Table 3. additional Cu supplements, or alternative feeds. The

Leaching of Mo at a particular site will be influenced common sense and practicality of good pasture and ani-by local climatic and management (irrigation leaching mal management should add significant confidence tofraction) factors, but should not be less than the 1.8% the risk assessment presented here.yr�1 assumed here except under acid soil pHs wheremolybdenum availability is low and Mo toxicity is un-

Uncertainties in the Risk Assessmentlikely. At high soil pH, where Mo availability and toxic-ity can be problematic, leaching should be greater than A weakness in the original USEPA risk assessment

was the limited animal (HEI) response database, espe-assumed here, and ignoring its influence on permissibleMo loads is unnecessarily and inappropriately conser- cially animals consuming forages grown on biosolids-

amended land. Much of the animal response data usedvative.


to justify low (�10 mg Mo kg�1 ) threshold intake (TPI) (species most susceptible to molybdenosis) allow calcu-lation of a diet-weighted UC factor that better repre-values, for example, were based on Mo salt additions

to diets of confined animals. There are very few studies sents forage Mo exposure to cattle. Recent biosolidsuse data allow estimating of the fraction of animal forageinvolving biosolids-Mo fertilized forage grazed by rumi-

nants (e.g., O’Connor and McDowell, 1999; K. Bro- likely to be grown on biosolids-amended land (FC) and,thus, a more reasonable estimate of possible biosolidsersma and W.C. Gardner, personal communication,

1999). Gardner et al. (1996) recently reported minimal Mo effect on animal diets. Data from both laboratoryand field studies show that biosolids Mo is not conservedresponses of cattle to grazed forages with total Mo con-

centrations of 20 to 40 mg Mo kg�1 and forage Cu to when land-applied and that estimates of Mo leaching(LC) are necessary to realistically assess long-term soilMo ratios �1. Forage (including legumes) was grown

on mine spoils with high pH (calcareous). Molybdenum Mo status.We incorporated these various improvements into aconcentrations in animal plasma and livers increased,

but there was no evidence of molybdenosis or detrimen- modified Pathway 6 algorithm as follows:tal effects in the animals. Cattle supplemented with Cu

RPc � (RC/UC) � (1/FC) � (1/LC)had the same adequate Cu in plasma and livers, andthe same overall health, as nonsupplemented cattle. For- where RF � 9, UC � 2.25, FC � 0.2, and LC � 0.45.age S concentrations were apparently low (but normal: This algorithm results in a cumulative biosolids Mo�2 g kg�1 ) in their study, and may have minimized application limit (RPc ) of 40 kg Mo ha�1 and a corre-thiomolybdate (or direct cupric sulfide) formation. sponding alternate pollutant concentration (Table 3 ofAlso, Loneragan et al. (1998) noted that high Mo could Part 503) of 40 mg Mo kg�1. We regard our modifica-decrease ruminal production of sulfide. Thus, there may tions and calculations as conservative, and believe theactually have been too much Mo in the forage to pro- risk of Mo toxicity from biosolids Mo is small in themote adequate sulfide, and thiomolybdate, formation vast majority of situations. Normal good pasture andin the Gardner et al. (1996) study. Canadian researchers animal management (especially, providing adequate Cu(K. Broersma and W.C. Gardner, personal communica- mineral supplementation) would complement the con-tion, 1999) hypothesize that forage Mo is somehow un- servatism of the risk assessment presented here.available for reaction in the ruminants, an effect similarto reduced Mo availability when forage is dried (Alla- ACKNOWLEDGMENTSway, 1977). Research into the form of Mo in the forage

Many people provided invaluable input to this effort. Some,and the effects of increased S in the diets is underway.for example, J.T. Artiola, N.T. Basta, K. Broersma, W. Gard-Animals are being grazed on leguminous forages grownner, T.C. Granato, and M. McBride provided critical dataon biosolids-amended land (K. Broersma and W.C. (unpublished at the time) for consideration. These and others

Gardner, personal communication, 1999). (notably J. Ryan, T.J. Logan, and R.H. Dowdy) offered in-Forages grown on biosolids-amended soil frequently sightful comments to the modified algorithm development.

have increased S contents (Nguyen, 1998; O’Connor Too numerous to name are the many people who respondedand McDowell, 1999; McBride et al., 2000). Low-main- to phone calls and emails from the senior author requesting

help to understand the system and normal agronomic andtenance pastures and rangelands are often underfertil-animal management practices, nationwide. We warmly thankized, and respond well to nutrient inputs provided inall who cooperated and rightfully accept responsibility for anybiosolids. Bahiagrass (Paspalum notatum flugge) (Ngu-misinterpretation of their input.yen, 1998; O’Connor and McDowell, 1999) was espe-

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a modified risk assessment to establish molybdenum standards for land application of biosolids

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