REVIEWS AND ANALYSES
A Modified Risk Assessment to Establish Molybdenum Standards
for 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
The USEPA standards (40 CFR Part 503) for the use or disposal
of sewage sludge (biosolids) derived risk-based numerical values for
Mo for the biosolids → land → plant → animal pathway (Pathway
6). Following legal challenge, most Mo numerical standards were
withdrawn, pending additional field-generated data using modern bio-
solids (Mo concentrations ⬍75 mg kg⫺1 ) and a reassessment of this
pathway. This paper presents a reevaluation of biosolids Mo data,
refinement of the risk assessment algorithms, and a reassessment of
Mo-induced hypocuprosis from land application of biosolids. Forage
Mo uptake coefficients (UC) are derived from field studies, many of
which used modern biosolids applied to numerous soil types, with
varying soil pH values, and supporting various crops. Typical cattle
diet scenarios are used to calculate a diet-weighted UC value that
realistically represents forage Mo exposure to cattle. Recent biosolids
use data are employed to estimate the fraction of animal forage (FC)
likely to be affected by biosolids applications nationally. Field data
are used to estimate long-term Mo leaching and a leaching correction
factor (LC) is used to adjust cumulative biosolids application limits.
The modified UC and new FC and LC factors are used in a new
algorithm to calculate biosolids Mo Pathway 6 risk. The resulting
numerical standards for Mo are cumulative limit (RPc) ⫽ 40 kg Mo
ha⫺1, and alternate pollutant limit (APL) ⫽ 40 mg Mo kg⫺1. We regard
the modifications to algorithms and parameters and calculations as
conservative, and believe that the risk of Mo-induced hypocuprosis
from biosolids Mo is small. Providing adequate Cu mineral supple-
ments, standard procedure in proper herd management, would aug-
ment the conservatism of the new risk assessment.
A pplication on agricultural land is the most common
beneficial use of biosolids today (National Re-
search Council, 1996), and pastures frequently represent
attractive application sites. For example, pastures in
Florida occupy ⬎5 million ha, are frequently underfertil-
ized, and respond well to nutrients (e.g., N, P, S, Fe)
G.A. O’Connor, Soil and Water Science Dep., and L.R. McDowell,
Dep. of Animal Science, Univ. of Florida, P.O. Box 110510, Gaines-
ville, FL 32611. R.B. Brobst and A. Rubin, USEPA, 401 M St., SW,
Washington, DC 20460. R.L. Chaney, USDA/ARS, Beltsville, MD
20705. R.L. Kincaid, Dep. of Animal Sci., Washington State Univ.,
Pullman, WA 99164. G.M. Pierzynski, Dep. of Agronomy, Kansas
State Univ., Manhattan, KS 66506. G.G. Van Riper, Montgomery
Watson, Lakewood, CO 80228. Although employees of the USEPA
were involved in the preparation of this document, it has not had the
USEPA’s peer and policy review, and does not necessarily reflect the
views of the agency. Contribution of the Florida Agric. Exp. Stn.
Journal Ser. no. R-07599. Received 15 June 2000. *Corresponding
author (gao@ufl.edu).
Published in J. Environ. Qual. 30:1490–1507 (2001).
1490
provided by biosolids (O’Connor and McDowell, 1999).
Similarly, rangelands—the predominant land use in the
arid and semiarid western regions of the USA—offer
abundant acreages for land application of biosolids.
Aside from providing plant nutrients and enhancing soil
conditions, land application of biosolids can increase
plant cover, decrease runoff, and reduce erosion (Drae-
ger et al., 1999). Pastures and rangelands also typically
represent low-population areas that minimize aesthetic
problems and traffic issues associated with biosolids use.
Biosolids, however, also contain trace elements whose
fate must be considered in pasture and rangeland im-
provement programs involving land application. In 1993,
the U.S. Environmental Protection Agency (USEPA)
promulgated regulations (40 Code of Federal Regulations
[CFR] Part 503) that, coupled with state regulations, gov-
ern biosolids recycling (USEPA, 1994). The federal rule
is risk-based (to protect against reasonably anticipated
adverse effects), and assesses exposure of animals, hu-
mans, and the environment to biosolids-borne metals
through 14 pathways. One of the assessment pathways
pertinent to biosolids use on pastures and/or rangelands
(Pathway 6) evaluates metal transfer from biosolids →
soil → plants → animals. Exposure to molybdenum (Mo)
via Pathway 6 is critical because ruminants (especially
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 for
Mo in land application programs, and calculations of
allowable biosolids Mo loads to soils from the pathway
were used to set numerical standards for Mo in the
federal rule. The next most limiting pathway was Path-
way 3 (direct human consumption of soil), and yielded
a Mo limit ⬎20-fold greater than Pathway 6. Four tables
in the Part 503 rule define various types of pollutant
limits: Ceiling Concentrations in Table 1, Cumulative
Pollutant Loading Rates in Table 2, Pollutant Concen-
trations in Table 3, and Annual Pollutant Loading Rates
in Table 4. Molybdenum was included in all tables, with
numerical values of 75 mg Mo kg⫺1 (Table 1), 18 kg Mo
ha⫺1 (Table 2), 18 mg Mo kg⫺1 (Table 3), and 0.9 kg
Mo ha⫺1 yr⫺1 (Table 4).
Abbreviations: BC, background concentration of pollutant in forage;
FC, fraction of animal forage likely to be affected by biosolids applica-
tion; HEI, highly exposed individual; LC, leaching correction factor;
RF, allowable Mo increment in plant tissue; RPc, cumulative biosolids
application limit; TPI, threshold pollutant intake at which a toxic effect
is noted in animals consuming the forage; UC, uptake coefficient.
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
Climax Metals Company, and several other compa-
nies engaged in Mo production, use, and processing
activities, filed a petition with the United States Court
of Appeals for the 10th Circuit seeking a review of the
land application numerical limits for Mo. Petition review
was subsequently transferred to the Washington, DC
Circuit Court. The litigants claimed that the data used
in the critical pathway risk assessment were faulty, and
that the Mo numerical limits were, thus, overprotective
of public health and the environment. Litigants also
claimed that the USEPA had disregarded the basis of
a previous rule (USEPA, 1990) banning the use of hexa-
valent chromium (chromate) as an algaecide in comfort
cooling towers. In the proposal to the rule, the USEPA
recommended molybdate as a cost-effective and non-
toxic replacement for chromate (USEPA, 1988). The
USEPA agreed with the petitioners’ assertions, and sub-
sequently agreed to temporarily suspend the Mo numer-
ical limits for Tables 2 through 4 of 40 CFR, Part 503,
but retain the ceiling value of Table 1 (USEPA, 1994).
The Agency committed to reconsider its risk assessment
of Mo, including evaluating new data pertinent to the
effects of biosolids Mo land application. The USEPA
committed to formulate, and propose for public com-
ment, new Mo numerical standards for 40 CFR, Part
503 Tables 2 through 4 after this reevaluation (USEPA,
1994). The USEPA expects to propose new Mo stan-
dards in 2001, respond to public comments, and promul-
gate Mo standards for Tables 2 through 4 thereafter (A.
Rubin, personal communication, 2000).
This document represents the reevaluation of biosol-
ids Mo data and risk assessment. We begin with brief
reviews of Mo sources and uses and Mo toxicity. We
then address recent data for Mo in biosolids and, finally,
consider Mo risk assessment. The latter effort includes
a review of the initial risk algorithms and their parame-
ters, and updated databases pertinent to their use. We
then offer a new algorithm, and provide data for its use
to calculate Mo numerical standards.
Sources and Uses of Molybdenum
Molybdenum was not described chemically until the
late 18th century, but its use had been documented as
early as the 14th century (International Molybdenum
Association, 1999). Steel and cast iron production is the
largest user (⬎75% of the Mo produced), but Mo is also
used in the manufacture and use of pigments, catalysts,
lubricants, corrosion inhibitors, and fertilizer (Interna-
tional Molybdenum Association, 1999).
Besides Mo in food and feces, the most common
source of Mo discharged to sewer systems is from com-
fort cooling towers, where water is used as a recirculat-
ing cooling medium in the towers. Chemicals are added
to control corrosion, mineral deposition, scaling, and
bacterial and algae growth (Bastain and Brobst, 1993).
Molybdenum Toxicity
An extensive review of Mo requirements, toxicity,
and nutritional limits for humans and animals (Ward,
1994) is recommended for those desiring more detail
1491
Table 1. Summary of Mo analytical results from the 1988 national
sewage sludge survey of waste treatment plants (USEPA,
1990b).
Treatment No. Percent Mean Standard
plant capacities samples detection concentration deviation
mg kg⫺1
⬎4.38 m3 s⫺1
(⬎100 MGD)† 26 69 8.08 6.10
⬎0.438⬍4.38 m3 s⫺1
(⬎10⬍100 MGD) 61 77 12.98 17.18
⬎0.044⬍0.438 m3 s⫺1
(⬎1⬍10 MGD) 70 66 10.31 11.05
⬍0.044 m3 s⫺1
(⬍1 MGD) 42 48 8.89 17.54
National 199 53 9.24 16.58
† MGD, million gallons per day.
than offered here. Molybdenum toxicity (molybdenosis)
was first identified in 1938 as the cause of severe diar-
rhea and emaciation in cattle-grazing areas called teart
pastures in England. In the same reference, Ferguson
et al. (1943) reported that the problem could be cor-
rected by copper sulfate addition to diets. Clinical signs
of a Mo-induced Cu deficiency in ruminant animals,
such as cattle and sheep, are exacerbated by increased
S in the diet. Severe Mo toxicity signs in cattle include
debilitating diarrhea leading to emaciation, loss of
weight, and sometimes death. Mild Mo-induced hypo-
cuprosis may be expressed by hair color changes (achro-
motricia). A direct effect of Mo on animal reproduction
has also been demonstrated (Phillippo et al., 1987).
Cattle appear to be the most susceptible species to
Mo toxicity, followed by sheep. Horses grazed the teart
pastures of England with no clinical signs of Mo toxicity.
Differences in susceptibility among species are usually
interpreted to suggest that processes in the rumen en-
hance the toxicity of Mo by reducing the availability
of Cu. However, ruminants like mule deer and goats
tolerate up to 1000 mg Mo kg⫺1 diet, about the same
as chickens, rabbits, and rats (Ward and Nagy, 1977;
Anke et al., 1985).
No clear evidence of Mo toxicity has been reported
in humans (Frieberg et al., 1975), but Ward (1994) rea-
soned that human tolerance would be expected to be
much higher than for cattle or sheep, as is the case for
all nonruminant species studied.
Copper intake is the primary interaction factor in
Mo toxicity because sufficient Cu supplementation can
counteract almost all disorders associated with high Mo
intakes (Clawson et al., 1972). Ward (1994) identified
dietary factors clearly related to Mo-induced hypo-
cuprosis as Cu intake, Cu availability, S intake, Fe in-
take, and the physical form of the feed.
Dietary Cu is poorly absorbed in most animal species,
although absorption is greater in young than mature
animals and in Cu-deficient than Cu-sufficient animals.
Mature sheep absorb less than 10% of the Cu ingested
(Suttle, 1973). Often, only 1 to 3% of dietary Cu is ab-
sorbed in ruminants. The Cu availability in cereal grains
may be 10 times greater than in forages (Suttle, 1986).
This partially explains why Cu deficiency can be a prob-
lem with grazing bovines, but usually not with dairy
cattle or finishing cattle that receive greater amounts
of concentrates in their diets.
 1492
Table 2. Data used to estimate Mo uptake coefficients (UC values) for various crops.
Study Soil Mo Tissue Mo Uptake
type† Plant, tissue Soil pH load‡ concentration coefficient§ Reference Comments
kg ha⫺1 mg kg⫺1
Forage nonlegumes
A corn, stover NR¶ 0–9.7 0.24–0.67 0.04 Soon and Bates (1985) Ca-enriched biosolids Soil Mo loads calculated
from initial biosolids loads.
A NR 0–6.1 1.0–3.7 0.44
A NR 0–10 0.24–0.28 0.004 Fe-enriched biosolids
A NR 0–12 1.0–0.65 0.001# Point estimates of UC.
A NR 0–12 0.24–0.28 0.003 Al-enriched biosolids
A NR 0–13 1.0–0.72 0.001#
A corn, stover 7.8 0–2.4 0.28–0.29 0.004 O’Connor et al. (2001b) Fulton County long- Soil Mo load calculated
term plots, 1975 from soil Mo concen-
tration each year.
Continuous corn.
A 7.8 0–4.0 0.28–0.29 0.002 1977
A 7.8 0–7.3 0.34–0.38 0.006 1981
A 7.8 0–10.5 0.36–0.18 0.001# 1985
A 7.8 0–13.7 0.13–0.15 0.002 1989
A 7.8 0–16.9 0.32–0.29 0.001# 1993
A 7.8 0–20 0.21–0.16 0.001# 1997
A corn, stover 7.8 0–20 0.13–0.38 0.001# 1975–1997 average
A corn, stover 6.2–6.6 0–0.65 0.51–0.38 0.001# O’Connor et al. (2001b) Rosemont Experiment Soil Mo load calculated
from soil Mo concen-
1977 continuous tration each year.
A 6.2–6.6 0–1.4 0.42–0.51 0.001# 1979 corn
A 6.2–6.6 0–1.0 0.89–3.0 0.79 1995 corn following soybeans
A corn, stover 6.2–6.6 0–1.4 0.4–3.0 0.19 Pooled 1977, 1979, and
1995 data
A winter wheat 6.7 0–2.0 0.2–1.0 0.24 Basta et al. (1999) Soil Mo load calculated
from soil Mo concentrations.
A bahiagrass 5.0–5.9 0–2.2 0.1–3.0 0.50 O’Connor and McDowell Soil Mo loads calculated from soil Mo concentration each year.
(1999) Plant Mo represents yield-weighted average over several
harvests each year. Multiple biosolids sources. Three-year
study (data pooled).
A bahiagrass 5.7–6.9 0–1.0 0.7–10 4.6 Nguyen (1998) Lower Fe ⫹ Al bio- Soil Mo loads calculated
from soil Mo concentration
J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001

solids Years 1 ⫹ 2
pooled each year. Plant Mo repre-
sents yield-weighted average
over several harvests. Two-
year study.
A 5.5–6.5 0–1.0 0.7–4 0.39 Higher Fe ⫹ Al bio-
solids Years 1 ⫹ 2
pooled
A bromegrass NR 0–4.1 0.38–1.9 0.36 Soon and Bates (1985) Ca-enriched biosolids Soil Mo loads calculated
from initial biosolids loads.
Plant Mo represent means
of two cuttings.
A NR 0–9.4 0.38–0.70 0.03 Fe-enriched biosolids
A NR 0.11 0.38–1.2 0.07 Al-enriched biosolids
Point estimates of UC
Continued next page.
Table 2. Continued.
Study Soil Mo Tissue Mo Uptake
type† Plant, tissue Soil pH load‡ concentration coefficient§ Reference Comments
kg ha⫺1 mg kg⫺1
Grains, cereals
A corn, grain NR 0–9.7 0.13–0.25 0.012 Soon and Bates (1985) Ca-enriched biosolids Soil Mo loads calculated
from initial biosolids loads.
A NR 0–6.1 0.25–0.73 0.08
A NR 0–10 0.13–0.17 0.004 Fe-enriched biosolids
A NR 0–12 0.25–0.25 0.001
A NR 0–12 0.13–0.18 0.004 Al-enriched biosolids Point estimates of UC.
A NR 0–13 0.25–0.29 0.003
Legumes
A soybean, grain 4.6–5.3 0–66 14.3–122 1.6 Pierzynski and Jacobs (1986) Year 1, Experiment 1
A 4.7–6.4 0–141 8.9–241 1.7 Year 2, Experiment 1
A 5.0–6.9 0–141 19.9–56.4 1.6 Year 3, Experiment 1
A soybean, grain 7–8 0–18 0.2–70.0 1.7 O’Connor et al. (2001a) Long-term biosolids appli- Soil load calculated from soil
cation (cumulative Mo concentration in 0–15
loads 苲650 Mg ha⫺1 ). cm depth.
Point estimates of six
plots used to cal-
culate mean.
A soybean, 4.6–5.3 0–66 2.7–56.4 0.81 Pierzynski and Jacobs (1986) Year 1, Experiment 1 Identified whole plant as sample
whole plant type.
A 4.7–6.4 0–141 3.1–321 2.3 Year 2, Experiment 1
A 5.0–6.9 0–141 5.4–459 3.2 Year 3, Experiment 1
A soybean, leaf 4.6–5.3 0–66 2.1–52.8 0.77 Pierzynski and Jacobs (1986) Year 1, Experiment 1
A 4.7–6.4 0–141 2.4–268 1.9 Year 2, Experiment 1
A 5.0–6.9 0–141 9.3–452 3.2 Year 3, Experiment 1
B soybean, 6.0–6.6 40–188 300–986 4.2 Pierzynski and Jacobs (1986) Second cutting Identified whole plant as sample
whole plant type. Soil Mo concentra-
tions multiplied by two to
give loadings.
B 7.0–7.5 40–188 736–1070 2.0
B 7.7–8.2 40–188 391–692 1.9
B soybean, 6.0–6.6 63–300 300–986 2.6 Pierzynski and Jacobs (1986) Second cutting Identified whole plant as sample
whole plant type. Calculated slopes using
actual loading rates from field
study used as source of soil
O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS

for greenhouse study.

B 7.0–7.5 63–300 736–1070 1.3
B 7.7–8.2 63–300 391–692 1.2
B alfalfa 6.0–6.6 40–188 201–659 2.9 Pierzynski and Jacobs (1986) Second cutting Soil Mo concentrations
multiplied by two to give
loadings.
B 7.0–7.5 40–188 487–895 2.4
B 7.7–8.2 40–188 483–944 2.9
Continued next page.
1493
1494 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001

Copper bioavailability in forages is greatly influenced

§ For plant tissue data sets with more than two application rates, a linear regression was used to determine the slope. Application rate was the independent variable. For those with only two applications
Soil Mo loads calculated from
Calculated slopes using actual

study used as source of soil

by forage levels of S and Mo and, to a lesser degree,

solids Mo concentration.
biosolids load times bio-
loading rates from field
by forage Fe, Zn, and Cd levels. In the presence of S,

for greenhouse study.

Point estimates of UC.

high intakes of Mo can induce a Cu deficiency due to
formation 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 pathways
exist by which Cu ⫻ Mo ⫻ S interactions mediate Cu
deficiency (Dick, 1956; Ryan et al., 1987). Sulfur also
Comments

rates, the tissue concentration of the control was subtracted from the concentration of the nonzero application rate and the difference was divided by the application rate.
exerts an independent effect on the availability of Cu
to ruminants, and the effect of S alone may be greater
Alkaline-stabilized sludge than the S-dependent effects of Mo (Underwood and
Suttle, 1999). Sulfides react with molybdate in the reduc-
ing medium of the rumen to replace oxygen, producing
thiomolybdates. These concepts of Mo–Cu antagonism
Dewatered sludge
Second cutting

in ruminants envisage that Mo acts, not by direct interac-

tion with Cu, but as a secondary consequence of Mo
affinity for sulfide generated within the rumen. Ex-
cessive quantities of dietary S (⬎3 to 4 g kg⫺1 ) as sulfate
or elemental sulfur may cause toxic effects and, in ex-
treme cases, can be fatal (Kandylis, 1984). The effects
of soil ingestion and Fe excess on Cu absorption (Suttle
Pierzynski and Jacobs (1986)

et al., 1975; Suttle et al., 1984) are believed to result

from Fe binding of sulfide in the rumen, with subsequent
McBride et al. (2000)

release of sulfide in the intestine that interferes with

Reference

Cu 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-
Legumes

lism. The tolerable risk threshold of Cu to Mo ratio in

feed is not fixed, but declines from 5:1 to 2:1 as pasture
Mo concentrations increase from 2 to 10 mg kg⫺1 (Suttle,
1991). Alloway (1973) suggests that the critical Cu to
coefficient§
Uptake

Mo ratio is 4:1, whereas Miltimore and Mason (1971)

1.8

1.5
1.8
1.1

4.3

suggest a narrower ratio of 2:1. Inclusion of S in the

interaction is preferable to use of only Cu to Mo ratios,
but this consideration has not been reduced to a field-
validated formula or ratio.
concentration

For grazing bovines, the problem of Cu deficiency

Tissue Mo

0.57–6.69

0.57–18.5
kg⫺1

201–659

437–895
483–944

due to low forage Cu or a conditioned Cu deficiency

mg

(e.g., high forage Mo and/or S) is restricted to the usual

six-month season for grazing of green forages. The con-
dition is rarely seen during the feeding of stored forages
in either beef or dairy cattle. Copper deficiency can be
Soil Mo

ha⫺1

63–300

63–300
63–300

highly detrimental for cattle grazing fresh forage in some

load‡

0–5.8

0–4.2

regions, but when this same forage is dried as hay, there

‡ Reported application rate unless otherwise noted.
kg

Default UC ⫽ 0.001 when slopes are negative.

is no Cu deficiency (Huber et al., 1971; Allaway, 1977).

These authors suggested that drying forage makes Cu
more available for absorption and reduces the availa-
† A ⫽ field study, B ⫽ greenhouse study.
Soil pH

6.0–6.6

7.0–7.5
7.7–8.2
6.5–7.0

苲8

bility of Mo.
Suttle (1980) evaluated Cu bioavailability of grazed
pastures, dried grass, hay, and silage by responses in
plasma Cu during repletion of hypocupremic ewes. Cop-
Plant, tissue

per in cut hay and grass was more bioavailable than Cu

Table 2. Continued.

red clover

¶ NR ⫽ not reported.

in fresh grass and silage from the same field. Copper

alfalfa

absorption in fresh grass ranged from 0.5 to 2.8% in

three of the four grasses. Copper absorption was 0.9 to
1.9% for grass silage, 3.1 to 4.9% for dried grass, and
5.2 to 7.2% for hay.
Study
type†

Bioavailability of Cu is affected by the genetics of

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

B
B
B

*
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS 1495

Table 3. Base information used on the calculation of fraction of diet affected (FC).
Total Crop, Pasture, Total Biosolids Land Pasture Weighting Weighted
States in farms† pasture range pasture‡ produced§ required¶ affected# factor†† FC‡‡
Column
A B C D E F G H I J
3 3 3
10 ha 10 Mg 10 ha %
AL 3 523 643 430 1 073 47 9 0.88 62 0.54
AK 357 3 265 269 15 3 1.1 0 0.00
AZ 10 873 47 9 584 9 631 43 9 0.09 100 0.09
AR 5 813 813 593 1 406 28 6 0.39 60 0.24
CA 11 210 504 5 821 6 326 720 144 2.3 77 1.7
CO 13 207 284 8 071 8 355 60 12 0.14 100 0.14
CT 145 11 8 19 83 17 88 26 23
DE 235 4 2 7 22 4 66 100 66
FL 4 231 362 1 647 2 010 253 51 2.5 100 2.5
GA 4 319 438 332 770 274 55 7.1 42 3.0
HI 582 17 364 381 17 3 0.90 14 0.12
ID 4 788 330 1 857 2 188 32 6 0.29 100 0.29
IL 11 010 334 273 607 474 95 16 89 14
IN 6 115 251 147 399 297 59 15 89 13
IA 12 613 810 583 1 393 98 20 1.4 100 1.4
KS 18 652 1 390 5 691 7 081 100 20 0.28 100 0.28
KY 5 396 1 255 456 1 712 47 9 0.55 18 0.10
LA 3 188 340 407 747 60 12 1.6 60 0.97
ME 490 26 11 38 19 4 10 89 8.9
MD 872 60 39 99 172 34 35 100 35
MA 210 16 10 26 203 41 160 33 52
MI 3 995 195 76 271 402 80 30 47 14
MN 10 520 404 383 787 47 9 1.2 90 1.1
MS 4 097 455 378 833 45 9 1.1 100 1.1
MO 11 666 2 124 1 504 3 627 250 50 1.4 53 0.72
MT 23 718 651 15 368 16 019 10 2 0.01 38 0.00
NE 18 424 745 8 853 9 598 64 13 0.13 100 0.13
NV 2 594 105 2 118 2 223 39 8 0.35 36 0.12
NH 168 9 6 15 18 4 25 48 12
NJ 337 26 14 40 236 47 120 47 55
NM 18 530 237 16 486 16 724 19 4 0.02 60 0.01
NY 2 936 256 192 448 340 68 15 47 7.1
NC 3 692 357 156 513 170 34 6.6 100 6.6
ND 15 929 580 4 200 4 779 9 2 0.04 100 0.04
OH 5 707 343 233 576 330 66 11 60 6.9
OK 13 443 2 016 6 245 8 261 50 10 0.12 100 0.12
OR 7 062 368 3 911 4 279 98 20 0.46 100 0.46
PA 2 901 276 151 426 464 93 22 100 22
RI 22 2 1 3 32 6 220 9 20
SC 1 859 206 99 305 118 24 7.7 45 3.5
SD 17 950 932 9 546 10 478 13 3 0.02 100 0.02
TN 4 501 990 398 1 388 96 19 1.4 100 1.4
TX 53 140 4 824 34 833 39 657 268 54 0.14 83 0.11
UT 4 866 226 3 742 3 968 16 3 0.08 39 0.03
VT 511 53 34 87 13 3 2.9 100 2.9
VA 3 330 615 435 1 050 235 47 4.5 75 3.4
WA 6 143 204 2 001 2 205 75 15 0.68 100 0.68
WV 1 398 266 214 480 20 4 0.83 100 0.83
WI 6 030 388 286 6 744 156 31 4.64 100 4.6
WY 13 796 298 12 162 12 460 3 0.6 0 100 0
US 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
absorption of minerals from the diet, varying from 2 to
10% for Cu in adult sheep (Field, 1981). When different
breeds of sheep grazed certain pastures in Scotland, one
breed exhibited signs of Cu poisoning, whereas another
showed signs of Cu deficiency (Wiener and Field, 1969).
Goonerante et al. (1989) reported that Cu deficiency in
Simmental cattle from Canada was more frequent than
in other breeds. Feeding high levels and combinations
of Cu, Mo, and/or S resulted in greatly enhanced biliary
Cu excretion in Simmental versus Angus cattle.
Underwood (1981) suggested that Mo is readily and
rapidly absorbed from most diets. Hexavalent water-
soluble forms, sodium and ammonium molybdate, and
the Mo of high-Mo herbage, most of which is water
soluble, are particularly well absorbed by cattle (Fergu-
son et al., 1943). Absorption of Mo from the disulfide
(MoS2 ) is poor, owing to low solubility and the antago-
nistic effect that S has on Mo absorption. Molybdenum
absorption depends on animal species, age, and level of
Mo in the diet, but the average value is 20 to 30%
based on experiments involving stable and radioactive
1496 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001
Table 4. Estimates of Mo leaching rates.
Study k Climate conditions
% Mo leached
Phillips and Meyer, 1993 1.86†
McBride et al., 1999 4.0
Nguyen, 1998 12.5
Hornick et al., 1977 1.8
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
is rapidly absorbed, but very rapidly excreted, mainly
in the urine and in part through the bile. High Mo
forages (11 to 32 mg kg⫺1 ) grown on soils containing
reclaimed mine tailings in Canada had little effect on
Cu status of grazing cattle, suggesting low bioavailability
of Mo (Gardner et al., 1996).
Rates of Mo absorption, retention, and excretion are
inversely related to the level of dietary S. In sheep, for
instance, increasing the dietary S from 1 to 3 g kg⫺1 in
a diet supplemented with 10 mg Mo per day decreased
the Mo retention from 37 to 4%. A working hypothesis
for the effect of S on Mo retention is that sulfate inhibits
membrane transport of molybdate, thus decreasing ab-
sorption of Mo in the intestine and decreasing reabsorp-
tion of Mo by the renal tubules (Dick, 1956; Ryan et
al., 1987). For sheep with a Mo intake of 0.3 mg d⫺1,
total body Mo decreased from 92.9 to 16.8 mg when
sulfate was increased from 0.9 to 6.3 g d⫺1 (Dick, 1956).
Molybdenum Concentrations in Biosolids
In 1988, the USEPA undertook a major effort to char-
acterize biosolids chemical composition for use in estab-
lishing the numerical pollutant limits in the final Part
503 rule (USEPA, 1990). The National Sewage Sludge
Survey (NSSS) data collection effort began in August
1988, and was completed in September 1989. The
USEPA collected biosolids from 177 wastewater treat-
ment plants and analyzed them for 419 analytes, or
pollutants, including Mo. Multiple samples were col-
lected at some treatment works to characterize the dif-
ferent types of biosolids end products. The NSSS mean
national concentration for Mo was 9.24 mg kg⫺1, with
a standard deviation of 16.6 mg kg⫺1 (Table 1). Many of
the detection limit problems (e.g., low percent detected)
have been attributed to analytical problems (Bastain
and Brobst, 1993).
Numerous studies (e.g., Logan, 1997) report that con-
centrations of most metals in modern biosolids are now
lower than in biosolids sampled for the NSSS. An excep-
tion is Mo, the concentration of which increased until
the early 1990s (Logan, 1997). Historical and modern
Mo data compiled by Brobst (R.B. Brobst, personal
communication, 2000) suggest an effect of national regu-
lations on biosolids Mo concentrations. Sales of molyb-
dates decreased 苲25% following promulgation of Part
503 in 1993 as publicly owned treatment plants (POTWs)
attempted to reduce biosolids Mo concentrations to
meet the proposed Table 3 pollutant concentration
value of 18 mg kg⫺1. Control of Mo discharges to sani-
tary sewers is achieved through local limits in the POTW
yr⫺1
California, irrigated. Low rainfall, circumneutral pH.
Eastern U.S. moderate rainfall, pH 7–7.3.
High rainfall, pH 5.5–6.9.
Eastern U.S. moderate rainfall, circumneutral pH.
pretreatment program. The concentration of Mo in bio-
solids in many regions of the USA began to decrease
quickly to the 20 mg Mo kg⫺1 mean (and 75% tile) con-
centrations seen today.
RISK ASSESSMENT
Molybdenum-Induced Copper Deficiency
The limiting risk assessment pathways pertinent to
Mo issues associated with land application of biosolids
is Pathway 6 (biosolids → soil → plants → animals).
The original USEPA assessment of molybdenosis risk
calculated the allowable, long-term biosolids Mo con-
centration in soil from the algorithm (USEPA, 1992):
RPc ⫽ RF/UC
where RPc ⫽ cumulative biosolids application limit (kg
Mo ha⫺1 ); UC ⫽ linear uptake slope of forage [(mg
Mo kg⫺1 forage)/(kg Mo ha⫺1 )] from biosolids-amended
soil; and RF ⫽ allowable Mo increment in plant tissue
(mg Mo kg⫺1 forage):
RF ⫽ TPI ⫺ BC
where TPI ⫽ threshold pollutant intake at which a toxic
effect is noted in animals consuming the forage (mg Mo
kg⫺1 forage) and BC ⫽ background concentration of
pollutant in forage (mg Mo kg⫺1 forage).
The initial risk assessment assumed: BC ⫽ 2.08 mg
kg⫺1, TPI ⫽ 10 mg kg⫺1, and UC ⫽ 0.423, resulting in
RPc ⫽ 18 kg ha⫺1.
Background Concentration (BC)
The USEPA selected the BC value of 2.08 mg Mo
kg⫺1 from the Pierzynski and Jacobs (1986) study, but
this represents a very high background concentration
for forages grown in low Mo (uncontaminated) soils.
Numerous recent literature citations for forages world-
wide (summarized in Kabata-Pendias and Pendias, 1991;
Gupta, 1997a; O’Connor and McDowell, 1999) suggest
that a more typical background value for Mo is almost
always ⬍1 mg kg⫺1. Plant Mo concentrations vary with
plant species, stage of development, plant part, soil pH,
soil drainage, soil Mo loads, etc., but uncontaminated
(naturally or anthropogenically), well-drained, non-
peat-like soils (normal organic matter contents) rarely
support plants with Mo concentrations ⬎1 mg kg⫺1,
and frequently result in Mo concentrations ⬍1 mg kg⫺1.
Legumes (e.g., alfalfa [Medicago sativa L.], clover [Tri-
folium pratense L.], soybean [Glycine max (L.) Merr],
etc.) can accumulate much greater concentrations (2
to 40 mg Mo kg⫺1 ) under natural conditions, but the
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
literature (e.g., Miltimore and Mason, 1971, and refer-
ences cited therein) suggests wide variations in legume
forage Mo contents, many ⬍1 mg kg⫺1, for areas as
diverse as British Columbia and Nevada. High soil pHs
and elevated natural soil Mo concentrations, or high
organic matter (peat), poorly drained soils that accumu-
late Mo from leaching (Kubota et al., 1961) typically
support vegetation with ⬎1 mg Mo kg⫺1. Such soils have
been mapped for the USA (Kabota, 1977), or are known
historically to produce high-Mo crops and to require
Cu supplementation of grazing animals (Allaway, 1977).
Such soils are not likely candidates for additional Mo
input via biosolids, unless special precautions are taken
to address Mo issues. For most soils, we believe that
BC can be realistically and conservatively estimated as
1 mg Mo kg⫺1, and that the USEPA should adopt the
lower value.
Threshold Pollutant Intake (TPI)
The threshold pollutant intake (TPI) value used ini-
tially by the USEPA was based on guidance from Na-
tional Research Council (1980), and was taken as 10 mg
Mo kg⫺1 animal diet. Ruminants are by far the most
susceptible herbivore to Mo-induced Cu deficiency, and
cattle are the most sensitive ruminants (Ward, 1994;
Suttle, 1991). Most references (Ward, 1994; Suttle, 1991;
McDowell, 1997; Gupta, 1997a) report TPI values that
range from a few (2 to 5) to tens (10 to 50) of mg kg⫺1,
and stress the importance of other issues (e.g., forage
Cu to Mo ratios, forage S content, age and condition
of the forage, degree of mineral supplementation of the
animals, etc.) as significant complicating factors. Unfor-
tunately, attempts to predict Cu–Mo–S–other elemental
interactions under field conditions have been largely
unsuccessful (Suttle, 1991).
The expert committee report of the National Acad-
emy of Sciences (National Research Council, 1980) eval-
uated low-level, chronic Mo toxicity, and identified “5
to 10 mg Mo kg⫺1, which has been weakly associated
with impaired bone development in young horses and
cattle” as the critical level. However, substantially
higher levels of Mo are tolerated in the presence of ade-
quate Cu and inorganic sulfate. Forages grown on bio-
solids-amended soils (high cumulative biosolids loads)
are typically normal (nondeficient) in Cu and sulfate,
so the higher permissible Mo concentration recommen-
dation of 10 mg Mo kg⫺1 seems appropriate. A large
body of data on the toxicity of Mo in forages grown on
soils naturally high in Mo (not Mo salt additions to
animal diets) supports the use of 10 mg Mo kg⫺1 for
forages with normal Cu concentrations in the diet (Na-
tional Research Council, 1980 [Table 1]; Suttle, 1991).
The TPI used by the USEPA represents the best avail-
able data for domestic animals, and may be considered
a lowest observed effect level (LOEL) rather than a no
observed adverse effect level (NOAEL). This distinction
is important, as other pathway analyses in Part 503 relied
on NOAEL values (when available) to build conserva-
tism into the risk assessment. Given the complexity of
Cu–Mo–S interactions, however, focusing exclusively on
1497
Mo without reasonable and practical considerations of
Cu and sulfate inputs in forage grown on biosolids-
amended soil and from normal mineral supplements
provided to grazing livestock seems unnecessarily re-
strictive. Ward (1994) concluded that it was nearly im-
possible to identify the equivalent of a NOAEL for Mo,
as the interactions surrounding Mo toxicity are too great
to establish the lower limit. He summarized numerous
data sets to conclude that 100 mg Mo kg⫺1 is definitely
toxic (molybdenosis, e.g., rapid scouring) to cattle, 25
to 50 mg kg⫺1 gives mixed results (sometimes no effect),
and that the Mo effects attributed to feeds with ⬍25 mg
Mo kg⫺1 are often associated with very low, and poorly
available, Cu. We conclude that using the higher end
of the NRC critical range (10 mg Mo kg⫺1 ) as the TPI
is justified.
The TPI is derived for domestic animals, as there are
few data for wild (nondomesticated) animals. Mule deer
reportedly tolerate up to 1000 mg Mo kg⫺1 in their diets
(Ward and Nagy, 1977). Flynn et al. (1977) hypothesized
a possible Cu ⫻ Mo ⫻ S interaction to explain abnormal
hoof material in moose, but acknowledged that their
overall data were consistent with the conclusions of
Kubota (1974) and others that “available information
does not suggest an existence of nutritional problems
in moose due to imbalances of Mo and Cu in feed
plants.” Domestic cattle may not be the most sensitive
animal to Mo toxicity, but there are no data to justify
selecting another species for use in the risk assessment.
Further, large, nondomesticated ruminant species typi-
cally graze large areas, and could be expected to receive
much less biosolids Mo exposure than domestic species
confined to biosolids-amended pastures.
Highly Exposed Individual
The risk assessment in Pathway 6 seeks to protect a
highly exposed individual (HEI), defined as “the most
sensitive/most exposed herbivorous livestock that con-
sumes plants grown on biosolids-amended soil. It is as-
sumed that 100% of the livestock diet consists of forage
grown on sewage sludge–amended land, and that the
animal is exposed to a background pollutant intake”
(USEPA, 1994). Grazing ruminants may, indeed, be
limited to forage growing on biosolids-amended land,
but dietary intake of common mineral supplements con-
taining Cu (that can obviate low Cu to Mo ratios of
forage) is ignored in the risk assessment. Further, con-
fined ruminants (finishing beef cattle or dairy cows) are
usually fed a variety of forages, grains, and mineral
supplements to maximize performance. How reasonable
is it to assume that 100% of the ruminant diet is one
kind of forage grown exclusively on biosolids-amended
land? What mitigating effects do supplemental Cu and
possible increased forage Cu (as a result of biosolids)
to the diet have on the risk of Mo-induced hypocu-
prosis? We examine the diet assumptions used to assess
Mo toxicity risk to ruminant livestock below.
Dietary Assumptions
Those livestock classified as ruminants include cattle,
sheep, and goats. Given the greater sensitivity of cattle
1498 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001
to Mo-induced hypocuprosis, we focus on cattle. Cattle
can be separated into beef and dairy because of the dif-
ferences in their feeding management. Risk assessment
for sheep and goats can be considered similar to either
dairy or beef cattle, depending upon their relative feed-
ing management.
Dairy Cattle. Feeding management of dairy cattle can
be divided into calves (0 to 3 mo), young heifers (3 to
6 mo), growing heifers (6 mo to breeding), pregnant
heifers (15 to 20 mo), lactating cows (305 d), and nonlac-
tating cows (60 d). Calves typically are born with high
concentrations of Cu (⬎300 mg Cu kg⫺1 of dry matter) in
their liver (Underwood, 1981) and these concentrations
decline over several months to those typical of adult
ruminants (Kincaid et al., 1986). Concentrates comprise
most of the dry feed for calves and young heifers; thus,
Mo-induced hypocuprosis is unlikely to occur in calves
and heifers because of the endogenous Cu reserves, use
of concentrates containing Cu supplements, and restricted
intakes of fresh forages in diets of these animals. Grow-
ing heifers (6 mo to breeding) are typically fed concen-
trates along with their forage. Once heifers are pregnant,
they are usually fed only forage and mineral supplements
until 2 to 4 weeks prepartum. Lactating dairy cows are
fed diets containing between 40 and 60% forage, and 60
to 40% concentrates (Ensminger et al., 1990). Concen-
trates for lactating cows consist of about 50% grain (e.g.,
corn [Zea mays L.] or barley [Hordeum vulgare L.]), 20%
by-product feeds (e.g., whole cottonseeds, beet pulp, and
wheat mill run), and 20% protein supplement (e.g., soy-
bean meal), with the remainder (10%) being molasses,
sodium bicarbonate, mineral supplements, vitamin sup-
plements, and various other ingredients.
The forage portion of dairy cow diets varies among
regions of the country (Mowrey and Spain, 1999). Often,
the forage consists of near equal proportions (dry matter
basis) of hay and silage during the nongrazing seasons,
to as much as 100% fresh forage during the 4- to 6-month
grazing season. The fresh forage can consist entirely of
grasses and legumes, although mixed pastures are most
common (Etgen et al., 1987). Regardless of the pasture
forage species, the entire ration of the dairy cow rarely
consists of more than 60% fresh legumes because of the
need to incorporate other feed ingredients into diets to
maximize milk production. Most large herds of dairy
cattle in the USA do not graze pastures, and their diets
remain fairly constant during all seasons of the year.
Nonlactating (dry) dairy cows are fed roughages until
14 d prepartum, when limited amounts of concentrates
are introduced into the diet to prepare the cows for the
lactation ration fed after parturition. Nonlactating dairy
cattle normally consume forages consisting of grasses or
legume–grass mixes, but are not fed 100% fresh legumes
because of possible health problems associated with ex-
cessive intakes of protein, energy, potassium, calcium,
and increased incidence of bloat (Etgen et al., 1987;
Ensminger et al., 1990). During the nonlactating period,
cows are provided mineral supplements.
Beef Cattle. Beef cattle production can be divided
into the cow–calf operation, stockers, and feedlot cattle.
Because feedlot cattle are fed high-concentrate diets
and slaughtered after about 120 d on feed, they are not
considered at risk for Mo-induced hypocuprosis. Beef
cattle are fed conserved roughages (hays, silages, and
crop aftermath) during the nongrazing seasons. During
the growing season, pastures for beef cows are domi-
nated by grasses, although variations exist among re-
gions in the USA. Legumes (alfalfa and clovers) are
often incorporated into pastures, but they rarely consti-
tute the entire ration of beef cows for extended periods.
Mixed plant species in a pasture assist in lengthening
the grazing periods and allow for plants that are best
suited to the soil conditions within a pasture (Etgen et
al., 1987). Young beef calves consume some fresh for-
age, and the amounts progressively increase as the calf
grows and the milk production of the dam declines.
Weaned beef calves (age ⬎ 259 d) may be fed only
roughage until they enter the feedlot for fattening. The
diets of these weaned calves (stockers) can include crop
residues (corn stalks, cereal grain straws, and stubble),
winter wheat (Triticum aestivum L.) (or other small
grain) pastures, irrigated pastures, silages, and hay (Ens-
minger et al., 1990).
The cattle groups perhaps at greatest risk of Mo-
induced Cu deficiency are beef cows, growing beef
calves, and pregnant heifers because of the dominance
of fresh forages in their diets. Attention to the concen-
trations of Mo, Cu, and S in their diets is needed and
especially to the trace mineral supplementation pro-
grams provided for these animals when Mo problems
are expected.
The risk of Mo-induced Cu deficiency is greatest dur-
ing the period of active growing forage, which is only 5
to 6 months in many areas of the country. Molybdenum-
induced Cu deficiency is not a problem for ruminants
receiving stored forages, apparently because of in-
creased availability of Cu and reduced availability of
Mo in these feeds (Underwood and Suttle, 1999). Most
important, Mo-induced Cu deficiency regions in the
USA are well known and farmers have learned to com-
pensate by providing Cu in mineral supplements (Alla-
way, 1977).
The use of a single TPI value of 10 mg Mo kg⫺1 is an
oversimplification of general animal response to forage
Mo exposure. Nevertheless, we believe that the TPI
value chosen is reasonable for a national risk assessment
for biosolids Mo when practical aspects of animal (HEI)
management (e.g., mineral supplementation and total
animal diet considerations) are recognized.
Allowable Molybdenum Increment (RF)
Based on the above discussion, the allowable Mo in-
crement in plant tissue (RF) is:
RF ⫽ TPI ⫺ BC
⫽ 10 ⫺ 1
RF ⫽ 9 mg Mo kg⫺1
To complete the risk assessment using the USEPA’s
original algorithm, RF is divided by UC to arrive at RPc.
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
Uptake Coefficient (UC)
Problems associated with appropriate selection and/
or calculation of UC values are many. Analytical prob-
lems with Mo (e.g., falsely high Mo analysis due to Fe
and Al interference and high limits of detection with
some methods; McBride et al., 2000) probably confound
interpretation of even some modern literature. Further,
many plant Mo uptake studies were conducted in the
greenhouse, and probably suffered greenhouse effect er-
rors (higher uptake slopes for contaminants compared
with those found in the field at similar contaminant
loads) discussed in the Part 503 Technical Support Doc-
ument (USEPA, 1992).
Ideally, the UC value is obtained from field experi-
ments where ranges of soil Mo loadings are evaluated.
In this case, UC is calculated as the slope of the linear
regression of plant tissue Mo concentrations (mg kg⫺1 )
versus biosolids Mo application (kg ha⫺1 ). The approach
implies that the plant tissue Mo response to soil Mo
load is linear and that the applied Mo remains in the
root zone indefinitely. The linear model was assumed
by the USEPA in the initial risk assessment for all metal
uptake calculations, but data in the Part 503 Technical
Support Document, and more recent data (e.g., Barbar-
ick et al., 1995) suggest a plateau model as more appro-
priate for at least some metals or crops. Limited data
presented by O’Connor and McDowell (1999) and Ngu-
yen (1998) suggest that the plateau model may also be
appropriate for biosolids Mo applied to a pasture grass.
Using a linear model when a plateau model is appro-
priate overestimates crop Mo (and risk) at higher bio-
solids application rates and over extended periods of
application. Given the incompleteness of the database,
a linear model is assumed herein.
Soil Molybdenum Load
Obtaining the plant Mo concentrations for the UC
calculations is relatively straightforward, but determin-
ing the soil Mo loading is less so. The most desirable
situation is to have measured total soil Mo concentra-
tions from a sampling time close to when the plants were
grown. These concentrations can then be converted to
soil Mo loadings (applied from biosolids) by multiplying
by the appropriate factor, considering sampling depth
and bulk density, and the background Mo concentration
in similar nonamended soil. For a sampling depth of 15
cm and a bulk density of approximately 1.3 Mg m⫺3,
one multiplies soil concentration by two to obtain soil
Mo loading in kg ha⫺1. This approach is consistent with
the assumption in the risk assessment that Mo is not a
conservative element in the soil. That is, if some time
has passed since the biosolids Mo was applied, leaching
may have reduced the soil Mo concentration to levels
lower than those predicted from the original Mo loading
rate (biosolids rate ⫻ biosolids Mo concentration). Un-
fortunately, few published studies report total soil Mo
concentrations for each of multiple cropping seasons,
and the original Mo loading rate must be used in the UC
calculation. In most studies, soil sampling and analysis is
restricted to the 0- to 15-cm depth, and ignores possible
1499
contribution of deeper soil profile Mo to plant uptake.
Thus, even if surface soil sampling occurs each year of
a multiyear study, soil Mo accessible to deep-rooted
plants may be underestimated. Another shortcoming of
many studies is the minimal range or number of soil
Mo loadings studied. Under these conditions, single-
point estimates of UC must be made. This is done by
subtracting the Mo concentration found in the control
(no added Mo) plants from the concentration in plants
grown on the biosolids-amended soil, and then dividing
by the biosolids Mo load.
Variations in Uptake Coefficient with Time
and Plant Part
Using point estimates of UC values is appropriate
for whole plant estimates of Mo exposure when, for
example, corn silage is fed, but not when perennial for-
ages are consumed. In such cases, UC values change
monthly (and widely) over an entire grazing season (e.g.,
Ferguson et al., 1943; Nguyen, 1998), with plant part
actually consumed (grains vs. stover, e.g., Gupta, 1997b),
and with forage condition (fresh vs. dried hay, e.g., Mills
and Davis, 1987). O’Connor and McDowell (1999) rec-
ommended calculating (yield) weighted average Mo
concentrations of grass grazed for 6 mo by cattle. The
weighted average concentration was thought to more
accurately represent the forage Mo concentration the
cattle experienced throughout the growing season than
simply calculating the average concentration of several
cuttings. The weighted average Mo concentration was
also thought to more reasonably represent the animal
forage consumption (Mo exposure) that varied with
grass yield throughout the grazing season.
Variations among Plant Species
Variations in plant species Mo concentrations—at the
same soil Mo load—are widely acknowledged (e.g.,
Gupta, 1997b; Vlek and Lindsay, 1977; Kabata-Pendias
and Pendias, 1991; Johansen et al., 1997) and, in fact,
form the basis for management of cattle Mo intake on
(known) high-Mo areas. Ranchers are advised to plant
nonaccumulating grasses or grains, rather than accumu-
lators such as legumes (e.g., alfalfa, clover, and soybean).
Miltimore and Mason (1971), however, cite several data
sets that show little difference in Mo concentrations in
grass, grass–legume, legume, or corn silage cattle diets
grown in areas as diverse as British Columbia, Canada,
Kansas, Virginia, and Nevada. Soil pH, wetness, Mo
concentration, and climate can all apparently play more
important roles in determining forage Mo concentration
than forage species alone. Nevertheless, legumes are
particularly susceptible to excessive Mo accumulation
(high uptake slopes), and databases used to assess Mo
toxicity should include legume UC values.
Variations with Soil Properties
Variations in plant-available Mo with soil pH are
well known (e.g., Gupta, 1997a,b; Kabata-Pendias and
Pendias, 1991; Pierzynski and Jacobs, 1986; Williams
1500 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001
and Gogna, 1981). High soil pH favors low Mo sorption
and high plant availability. Molybdenum adsorption en-
velopes typically exhibit maximal Mo sorption at soil
pH values ⬍5, so near-neutral and calcareous soils tend
to retain little Mo (e.g., Goldberg et al., 1996, 1998).
Most molybdenosis problems occur on such high-pH
soils (Allaway, 1977).
Variations in soil moisture and soil organic matter
contents affect plant Mo concentrations. Kubota et al.
(1963) showed that the same soil Mo concentration re-
sulted in vastly different plant Mo concentrations, de-
pending upon the soil moisture regime. Ready supply
of Mo in moist (poorly drained) soils is well recognized
(Kubota, 1977), and is one reason given for the abundant
Mo in plants growing in wet, high-organic soils (e.g.,
peats) even at relatively low soil Mo concentrations
(Allaway, 1977). In “normal” soils (well-drained, ⬍50 g
kg⫺1 soil organic matter), pH is usually the dominant
factor determining Mo phytoavailability. Soils with pH
values ⬎6 frequently result in forage with excessive
(10 to 20 mg kg⫺1 ) Mo concentrations if soil Mo concen-
trations are significantly above background levels (1
to 2 mg Mo kg⫺1 ) (Gupta, 1997a; Kabata-Pendias and
Pendias, 1991; Barber, 1984; Allaway, 1977).
Biosolids Source Effects
Biosolids source effects, based on excessively high
total biosolids Mo concentrations (e.g., Pierzynski and
Jacobs, 1986), or other constituents (Fe and Al) in the
biosolids (e.g., Soon and Bates, 1985; O’Connor and
McDowell, 1999) can also lead to vastly different UC
estimates. Such a biosolids effect was not directly con-
sidered in the original USEPA risk assessment, although
the Technical Support Document (USEPA, 1992) in-
cludes reference to data of Soon and Bates (1985) show-
ing lower Mo phytoavailability on soil amended with Fe
or Al biosolids compared with Ca biosolids amendment.
Ferric chloride and/or alum are routinely added in waste
treatment processes to improve P removal, and would
be expected to be similarly effective at immobilizing Mo.
Lime-stabilized biosolids can raise soil pH and increase
uptake slopes correspondingly (Soon and Bates, 1985;
McBride, 1998).
The original USEPA risk assessment included the
very high (1500 mg Mo kg⫺1 ) biosolids data of Pierzyn-
ski and Jacobs (1986), but data for such a biosolids (Mo
concentration 20-fold greater than the 98th percentile
of national biosolids) represent unique conditions. We
believe that the USEPA should omit the Pierzynski and
Jacobs (1986)-derived UC values when better data are
available.
The ideal data set for purposes of risk assessment
would be from field studies in which Mo was added at
various rates from biosolids containing less than 75 mg
Mo kg⫺1 (maximum biosolids Mo concentration allowed
for land application). In addition, having UC values for
all types of forages typically consumed by animals in
the exposure pathway of concern would be desirable.
Data for corn silage, stover, or grain would be preferable
to corn leaf diagnostic tissue data, for example. As pre-
viously mentioned, total soil Mo concentrations that
could be used to calculate Mo loadings would be prefer-
able to calculated Mo loadings based on biosolids com-
position and application rates. Few studies satisfy all
these criteria, and the selection of appropriate data sets
frequently requires use of professional judgement. One
essential requirement is that the UC values be generated
from studies in which biosolids were the Mo source.
Data from greenhouse pot studies would only be used if
no other data were available for a particular forage type.
The USEPA attempted to resolve the UC value varia-
tion issues by calculating a geometric mean of UC esti-
mates from a limited set of field- and greenhouse-gener-
ated data, where biosolids were the sources of Mo load.
The original Mo data set used in the 1993 rule devel-
opment was quite limited, but a few significant studies
(Basta et al., 1999; O’Connor and McDowell, 1999; Mc-
Bride et al., 2000; O’Connor et al., 2001a) that meet
most of the criteria described above are now available.
The data are included in Table 2, along with selected
data from Tables C-39, C-40, and C-41 of the Technical
Support Document (USEPA, 1992). Still underrepre-
sented in the table are data from field studies where
legumes are grown in biosolids-amended soils of high
pH, and where the biosolids have less than the ceiling
Mo concentration. A paper (O’Connor et al., 2001b)
describing one such set of soybean grain data has been
published; data are included in Table 2.
Uptake coefficients (UC values) of nonlegumes are
low and almost always ⬍0.5 (Table 2). The lone excep-
tion (UC ⫽ 4.6) in the database comes from a study
involving a pasture grass grown in soil amended with
one biosolids that was inadvertently overlimed in the
second year of a 2-yr study (Nguyen, 1998). Another
biosolids (slightly higher Fe and Al content) applied to
the same soil yielded a more representative UC value
for the grass of 0.39. The arithmetic average of the UC
values for 29 nonlegume entries in Table 2 is 0.24. We
conclude that a UC value for nonlegumes (vegetation
or grain) is conservatively estimated as 0.5.
Field data for estimating UC values for legumes are
limited, so greenhouse data (Pierzynski and Jacobs,
1986; McBride et al., 2000) are included in the database
(Table 2). The arithmetic average of UC values for 24
legume entries is 2.2. Given the limited diversity of
studies, we conclude that a UC value for legumes is
conservatively estimated as 4.0. No adjustment of the
UC value is made for the well-recognized decreased Mo
availability to cattle in dried (vs. fresh) forages (Mills
and Davis, 1987).
Based on the dietary considerations presented pre-
viously, we estimate that grazed fresh legumes will typi-
cally constitute no more than 50% of beef cattle or dairy
cow animal diets, and frequently less. The remainder of
the diets would typically consist of hay silage, roughage
(grain by-products), and grains, plus mineral supple-
ments. If an average UC value for fresh legumes is taken
conservatively as 4, and an average UC value for all
other plant-feedstuffs is taken very conservatively as
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 value
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
represents a worst-case estimate of typical forage Mo
exposure, and note that it ignores normal mineral (Cu)
supplementation recommended for good animal man-
agement.
Algorithm Modifications
Fraction of Diet Affected (FC)
Not all feed consumed by cattle is grown in the same
place, nor is all the land used to grow animal feed likely
to be biosolids-amended. It is particularly unlikely that
the feed-producing land would be amended every year
for a total application rate of 1000 Mg ha⫺1 (10 Mg ha⫺1
yr⫺1 ⫻ 100 yr), as was assumed in the risk assessment
(USEPA, 1992). More likely, the feed-producing land
would be amended at 5 to 10 Mg ha⫺1 (N-based applica-
tion rates) only periodically (e.g., once every 3 to 5 yr).
We examined biosolids production and use on crop and
pasture land in each state to estimate the fraction of
cattle diet (FC) likely to be affected by biosolids use.
Biosolids production is likely to remain the same or
increase only slightly over the next several years. Waste-
water treatment plant construction has slowed, and
increases in biosolids production are related to improve-
ments in existing treatment rather than new construc-
tion (Bastain, 1997). Estimates of biosolids production
and final use and disposal were surveyed in 1996; the
totals for the USA at that time were 6.8 ⫻ 106 dry Mg
produced, with 54% of the total being land-applied (Bas-
tain, 1997). Table 3 contains a summary of the quanti-
ties of biosolids produced and land-applied in each state.
Column B (Table 3) represents total acreage in farms
and ranches held as private lands in 1997 (USDA, 1999).
Column C represents land in crop rotation that, during
the year of the survey, was in pasture for at least part
of the year. Reviews of past USDA agricultural surveys
suggest that acreages in this category differ little from
year to year. Pasture and rangeland acreage (Column
D) represents lands remaining in pasture for several
years; generally considered permanent pasture. Past
USDA agricultural surveys (back to 1987) suggest simi-
lar acreages. Column E values are the total acreages in
pasture (Columns C ⫹ D), but do not include grazing
lands leased from government agencies. Addition of
these public lands would significantly increase the acre-
age, particularly in the 11 western states. Data for bio-
solids produced in each state (Column F) were summa-
rized by Bastain (1997). The values do not account for
intrastate transfer of biosolids, such as occurs from areas
with small land bases to areas with large land bases.
A biosolids load of 5 Mg ha⫺1 was chosen as a typical
application rate to pasture land, and was used to cal-
culate the acreage required to accommodate the load
(Column G).
Column H represents land required for biosolids ap-
plication (Column G) as a percentage of total land in
pasture (Column E). The calculation included all bio-
solids produced in each state, regardless of use and/or
disposal practice (e.g., land-applied, landfilled, or in-
cinerated), and all biosolids were assumed to be applied
to pastures, a conservative assumption. Brobst (R.B.
1501
Brobst, personal communication, 2000) conducted
an informal survey of contemporary biosolids use in
15 states, from Georgia to Oregon and from Minne-
sota to Arizona. Twelve of the states applied ⬍1% of
their biosolids to pastures; Oklahoma and Georgia ap-
plied ⬍10%, and Virginia applied 苲33%. Agricultural
producers tended to use the nutrients in biosolids on
croplands (rather than pastures) whenever possible to
reduce production costs associated with commercial
fertilizers.
The land application weighting factor (Column I) esti-
mates the possible increases in biosolids production and
the resulting fraction of land affected by land applica-
tion. Column I values were derived by multiplying the
percent of biosolids currently land-applied by 1.5, up to
a maximum of 100% of the biosolids produced. Column
J is the product of Column H and Column I, and repre-
sents a conservative estimate of pasture land (cattle
feed) likely to be affected by biosolids (FC). Twenty-
four states have FC values ⬍1%, 15 have values between
1 and 10%, 5 between 10 and 20%, and 6 have FC
values ⬎20%. None of the six states (Pennsylvania, New
Jersey, Connecticut, Delaware, Maryland, and Massa-
chusetts) was among the top 28 beef-producing states
in 1997 (USDA, 1999). We conclude that a reasonable
estimate of the fraction of ruminant forage likely to be
affected by biosolids (FC) is 0.1 to 0.2, and recommend
using the more conservative value of FC ⫽ 0.2 for a
national approach to rule making. The FC factor we
propose may not be universally applicable, but is consis-
tent with USEPA policy that estimates the fraction of
HEI diet probably affected by food grown on biosolids-
amended land in Pathways 1, 2, 4, and 5 (USEPA, 1992).
Local conditions may warrant using a different FC,
which would allow site-specific considerations in a bio-
solids land application program.
Leaching Correction (LC)
Maximum Mo loading considerations ignore the fact
that Mo is not a conserved element when biosolids are
applied to the same field for many years, especially to
soils having high soil pH where Mo leaching, bioavail-
ability, and risk are all maximized. Few studies have
been conducted with the primary objective of directly
characterizing Mo leaching dynamics and the parame-
ters affecting leaching rates. Nonetheless, several stud-
ies provide indirect evidence of Mo leaching from bio-
solids and industrial Mo sources. These studies are
summarized below, and demonstrate that Mo leaching
from the plow layer occurs, sometimes at high rates. Ad-
ditional studies of Mo leaching from biosolids sources
are recommended to develop a more complete data set
and to validate the approach used here.
Molybdenum is adsorbed by acidic soils, and exhibits
maximal retention at soil pH values ⬍5 (Goldberg et al.,
1996, 1998). O’Connor and McDowell (1999) presented
data for Mo sorption on biosolids-amended soils that
confirm Mo behavior noted by Goldberg for unamended
soils. Their data also confirm the dramatic reduction in
Mo retention as soil pH increases, with sorption becom-
1502 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001
ing negligible above pH 6. Thus, Mo availability to plants
(and to leaching) increases dramatically at higher pH.
Artiola (J.F. Artiola, personal communication, 1999)
conducted column studies with calcareous soils (pH ⫽
7.8) amended with biosolids Mo. The biosolids applica-
tion rate was about 200 Mg ha⫺1, and the New York
biosolids Mo concentration was 6 g Mg⫺1 (Mo load ⫽
1.2 kg Mo ha⫺1 ). Molybdenum moved through the col-
umns essentially unimpeded, and reached low relative
concentrations (C/Ci ⫽ 0.1) in drainage after only about
two pore volumes of drainage. There was little differ-
ence in Mo leaching behavior whether the Mo was
added as biosolids or Mo salts under such high-pH (7.8)
conditions. O’Connor and McDowell (1999) and Brin-
ton and O’Connor (2000) reported data that suggested
different effects of biosolids source on Mo retention
and/or release depending upon biosolids total Fe and
Al contents, but soil pH effects dominated Mo behavior
in two soils amended with the various biosolids. High
soil pH reduces soil retardation of Mo movement and
increases the likelihood that applied Mo will leach away
from the zone of biosolids incorporation. The effect
would be greatest under irrigated conditions, where net
downward flow of water is maintained (positive leaching
fraction) to control salinity. Chang and Page (2000) re-
cently conducted an input–output balance of trace ele-
ments in soils of the San Joaquin Valley’s West Side.
Numerous inputs were considered, including Mo from
biosolids additions. Despite the inputs from various
sources, there was a net depletion of Mo from cropland
on the West Side (Chang and Page, 2000). Amounts of
Mo dissolved from soils and transported to tile drains
exceeded amounts of Mo added from all input sources
combined. Leaching of Mo from these near-neutral soils
accounts for the net depletion of Mo, and is inevitable
for sustainable irrigated crop production (Chang and
Page, 2000).
Phillips and Meyer (1993) studied alfalfa growing in
calcareous (soil pH ⬎ 7) fields with natively high soil Mo
concentrations in Kern County, CA. An earlier (1950)
survey of alfalfa from the county had identified average
alfalfa tissue Mo concentrations of about 10 mg kg⫺1.
Resampling the same fields 35 yr later revealed average
alfalfa tissue Mo concentrations of about 3.5 mg kg⫺1.
No quantification of soil Mo concentrations was at-
tempted, but Phillips and Meyer concluded that the
lowered tissue Mo concentrations were associated pri-
marily with leaching of soluble salts (including Mo).
Similarly, McBride et al. (1999) reported that nearly
80% of biosolids Mo applied at high rates to a calcareous
silty clay loam (pH 7.0 to 7.3) had been lost from the
topsoil under natural rainfall conditions over the nearly
20 yr since the biosolids were applied.
Leaching of Mo is not restricted to high-pH soils.
Hemkes et al. (1980) applied moderate rates (6 to 18 Mg
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-
lands each year for 3 yr (total Mo loads ⫽ 2.1 to 9.2 kg
Mo ha⫺1 ). Molybdenum concentrations in the surface
(0–2.5 cm) soil reached 7.4 mg kg⫺1 at the greatest bio-
solids Mo load, and decreased with depth to background
concentrations at ⬎25 cm. They were unable to account
for all of the Mo added, and hypothesized Mo leaching.
Nguyen (1998) noted about 50% loss of biosolids Mo
from the surface 0- to 15-cm depth of a limed acid (pH
5.5–6.9) Spodosol 3 to 4 yr after biosolids application.
Thus, even slightly acid soils under high-rainfall condi-
tions can be expected to allow leaching of biosolids Mo.
Leaching would be promoted if the soils were limed
or amended with high-pH (alkaline-treated) biosolids
(McBride, 1998).
Leaching of Mo under nonirrigated, semiarid, or arid
conditions is often difficult to predict. Infiltration below
the root zone occurs when the magnitude and duration
of moisture events (e.g., snow melt, rainfall) exceed evapo-
transpiration, runoff, soil moisture retention, and ab-
sorption by surface materials (e.g., biosolids). McCurry
(1995) summarized infiltration data collected in several
states. Data represented infiltration studies on biosolids
projects in Colorado and New Mexico and basic infiltra-
tion studies conducted in New Mexico, Idaho, Califor-
nia, Texas, Oklahoma, and Utah. Infiltration data from
the biosolids studies were consistent with data collected
for nonbiosolids studies. Moisture infiltrated 40 to
⬎270 cm depending upon location and type of excess
moisture event (McCurry, 1995). Excess moisture in
arid and semiarid regions is usually only available in
the spring and early summer, following snow melt, and/
or for briefs periods following intense summer thunder-
storms. McCurry’s data demonstrate that water (and
dissolved ions) can move below the root zone during
these periods. Additional measurements of solute move-
ment through biosolids-amended soils under semiarid
and arid conditions have been made (Janonis et al.,
1996; Michalk, 1995; Moffet et al., 1995). Molybdenum
was not specifically monitored in either study, but is
expected to move as readily as other anions (e.g., PO4,
and SO4 ) whose migration was detected. Thus, leaching
of Mo can be expected in all but the driest of environ-
ments, and can be expected to be significant under
irrigated or high-rainfall conditions. Under dryland con-
ditions, salt accumulation typically limits biosolids ap-
plication rather than N, P, or Mo loads.
Leaching loss of Mo is expected to be greatest under
high soil pH conditions, where Mo bioavailability is
problematic. Not accounting for Mo losses to leaching,
even over the long periods (⬎100 yr) needed to attain
limiting cumulative soil Mo loads, is unrealistic.
Pollutant leaching can be characterized using rigorous
quantitative approaches or more qualitative approaches.
The USEPA, for example, used two transport models
(quantitative approach) to predict ground water effects
of land-applied biosolids-pollutants in the Pathway 12
and 14 (drinking water) risk assessment. The VADOF
subroutine of the RUSTIC model (USEPA, 1989) was
used to estimate flow and pollutant transport through
the unsaturated zone. A second model (AT123D; Yeh,
1981) was then used to estimate transport in the satu-
rated zone (aquifer). The combined model outputs esti-
mated pollutant transport to a receptor, a drinking water
supply well. Results of the simulations were used to
back-calculate reference pollutant application rates that
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
result in threshold ground water effects at the receptor
(USEPA, 1994). This rigorously quantitative approach
is data- and assumption-intensive, and is deemed inap-
propriate for Pathway 6 risk assessment for two reasons.
First, the receptor of interest in Pathway 6 (the most
sensitive pathway of risk for Mo) is a ruminant grazing
biosolids-amended forage, not a human drinking water
from a downstream well. Second, model parameters
were set to maximize pollutant leaching in Pathways 12
and 14 (USEPA, 1992), so risk in Pathway 6 is simultane-
ously underestimated (less Mo remaining in the soil for
plant uptake). For these reasons, we chose a simplified,
but conservative, model that uses a first-order leaching
algorithm and empirical data for pollutant leaching
characterization. The algorithm describes leaching that
annually removes Mo from the root zone in proportion
to the total Mo concentration in the soil (Eq. [1]):
dCy/dt ⫽ ⫺kCy [1]
where Cy is the Mo concentration (load) in soil (mg
ha⫺1 ) for any year, t is time (yr), and k is the leaching
percentage per year (% yr⫺1 ). The loss of Mo annually
due to leaching is represented by dCy/dt, and the concen-
tration of Mo in soil in any year (Cy ) is calculated as
the sum of Mo left after leaching the previous year
(Cy⫺1 ) and Mo added in the current year (Cadded ); Cy ⫽
Cy⫺1 ⫹ Cadded.
The model assumes relatively constant climatic condi-
tions over, for example, the maximum assumed 100-yr
biosolids application period. Further, one assumes a
constant pollutant addition rate and a constant (aver-
age) pollutant leaching rate (k). If no leaching is as-
sumed (k ⫽ 0), Mo accumulates in the soil in direct
proportion to the addition rate. When k ⬎ 0, the model
projects that the quantity of Mo leached will eventually
equal the quantity added, resulting in a steady-state
(plateau) soil Mo concentration (load). The plateau con-
centration depends on the annual Mo addition rate and
the assumed annual Mo leaching rate. The critical condi-
tion in the risk assessment for Pathway 6 is that the
plateau 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 is
typically nonlinear, with high initial rates, followed by
progressively slower rates in subsequent years as pollut-
ant mass decreases. We regarded constant linear rates
as appropriate for two reasons. First, biosolids additions
are incremental over the assumed 100-yr site life, which
better fits a constant, linear loss per year assumption.
If the entire cumulative biosolids load were applied in
one year, a nonlinear leaching model would be more
appropriate. Second, selection of an average (long-
term) annual loss rate results in less leaching estimation
in the short term (when soil Mo concentrations are
high), which leaves more Mo available for plant uptake.
Overall, we believe such assumptions are more protec-
tive of the Pathway 6 HEI.
We estimated long-term Mo leaching rates (k values)
from various literature sources mentioned previously.
Few published studies quantified annual Mo leaching;
1503
rather, most reported changes in soil Mo concentrations
many years after initial Mo contamination. The field
data are presented in Table 4, and do not include the
detailed laboratory data of Artiola (J.F. Artiola, per-
sonal communication, 1999), which suggest very high
biosolids Mo leaching rates under uniform, short-term
leaching conditions. Data in Table 4 represent estimated
annual Mo leaching rates of biosolids Mo (McBride et
al., 1999; Nguyen, 1998) and natural (Phillips and Meyer,
1993) or anthropogenic (Hornick et al., 1977) Mo
sources. The data represent leaching periods of 3 to 35
yr. The average leaching rate (k) for data in Table 4 is
about 5% yr⫺1, with a range of 1.8 to 12.5% yr⫺1. The
USEPA (1992) used a leaching rate of 12% yr⫺1 for As,
an anion expected to exhibit soil mobility similar to Mo.
Net soil Mo load (kg Mo ha⫺1 ) is calculated as a
function of time, assuming an application of 10 Mg ha⫺1
yr⫺1 of biosolids containing 40 and 75 mg Mo kg⫺1 at
1.8% yr⫺1 leaching (Fig. 1) and 5% yr⫺1 leaching (Fig.
2). Figure 1 predicts that a biosolids containing 40 mg
Mo kg⫺1 can be safely applied for 100 yr without ex-
ceeding the 20 kg Mo ha⫺1 diet-weighted (FC-corrected)
criterion when the smallest annual leaching rate (k ⫽
1.8% yr⫺1 ) is assumed. Figure 2 predicts that even a
biosolids containing the ceiling concentration of 75 mg
Mo kg⫺1 can be applied for 100 yr without exceeding a
plateau Mo load of 16 kg ha⫺1 when k ⫽ 5% yr⫺1. A
biosolids containing 40 mg Mo kg⫺1 could be applied
for 100 yr (at 5% leaching yr⫺1 ) and never exceed 8 kg
Mo ha⫺1, well below the soil load associated with Mo-
induced hypocuprosis, even when the dietary factor
(FC) is ignored. High soil pH exacerbates plant Mo
uptake, but also promotes Mo leaching, so long-term
Mo risk is minimized.
A leaching correction (LC) factor can be derived from
the figures by dividing the net soil Mo load remaining
Fig. 1. Net soil Mo load with time when soil is amended with biosolids
containing either 75 or 40 mg Mo kg⫺1 at 10 Mg biosolids ha⫺1
yr⫺1 and the leaching coefficient is either zero (no leaching) or
1.8% yr⫺1.
1504 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001
Fig. 2. Net soil Mo load with time when soil is amended with biosolids
containing either 75 or 40 mg Mo kg⫺1 at 10 Mg biosolids ha⫺1
yr⫺1 and the leaching coefficient is either zero (no leaching) or
5% yr⫺1.
after 100 yr by the total Mo load added. Thus, for a
biosolids containing 40 mg Mo kg⫺1 and at 1.8% leaching
per year (Fig. 1), the leaching correction factor is:
18 kg Mo ha⫺1 remaining
LC ⫽ ⫽ 0.45
40 kg Mo ha⫺1 added
and at 5% leaching per year (Fig. 2):
8 kg Mo ha⫺1 remaining
LC ⫽ ⫽ 0.2
40 kg Mo ha⫺1 added
We believe that a conservative correction for leaching
(LC ⫽ 0.45) makes the risk assessment appropriately
realistic, but recognize that a different LC value could
be necessary as additional field-scale leaching data be-
come available.
Incorporating Mo leaching considerations into the
Pathway 6 algorithm yields the following:
RPc ⫽ (RF/UC) ⫻ (1/FC) ⫻ (1/LC)
⫽ (9/2.25) ⫻ (1/.2) ⫻ (1/.45)
⫽ 44 kg Mo ha⫺1
Following the USEPA policy of rounding down criti-
cal limits, we derive an RPc value of 40 kg Mo ha⫺1,
and a corresponding alternate pollutant limit (APL) of
40 mg Mo kg⫺1 for Part 503 Table 3.
Leaching of Mo at a particular site will be influenced
by local climatic and management (irrigation leaching
fraction) factors, but should not be less than the 1.8%
yr⫺1 assumed here except under acid soil pHs where
molybdenum availability is low and Mo toxicity is un-
likely. At high soil pH, where Mo availability and toxic-
ity can be problematic, leaching should be greater than
assumed here, and ignoring its influence on permissible
Mo loads is unnecessarily and inappropriately conser-
vative.
Numerical Standards for Molybdenum
Based on the above considerations and the modified
algorithm presented, we suggest the following numerical
standards 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 Considerations
Animal 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 the
world (McDowell, 1992, 1997). Similarly, Mo-induced
hypocuprosis has been widely recognized as a problem
in selected areas of the USA, Canada, Europe, and
Australia for decades, and livestock owners have had
corrective management practices recommended to them
for ⬎50 yr (e.g., Lewis, 1943; Cameron and Goss, 1948).
The best primary management practice is to supplement
cattle feed with added Cu; typically, 10 mg Cu kg⫺1 of
diet, but increasing to 25 mg kg⫺1 during pregnancy,
and to as much as 50 mg kg⫺1 if “animals have access to
high sulfate water” (Gooneratne et al., 1989). Allaway
(1977) concluded that “stockmen in the USA have met
the problems of Mo toxicity by treating the animals,
rather than measures applied to the soil or crop. The
general utility of Cu therapy to prevent Mo toxicity has
minimized efforts to meet the problem through soil or
plant management.”
Thus, Mo-induced Cu deficiency problems are well
known, easily recognized, and easily corrected by
ranchers operating in areas prone to Mo toxicities.
Ranchers and farmers, who know from decades of expe-
rience that their soils produce crops prone to Mo accu-
mulation, are unlikely to intentionally add high Mo
loads via biosolids, or any other soil amendment, unless
this is done in conjunction with Cu supplementation.
Ranchers or dairymen receiving forage from elsewhere
are not likely to feed cattle excessive amounts of Mo-
accumulating plants (e.g., legumes) indiscriminately.
Imported forage is typically dry hay, which has a much
lower risk of Mo-induced hypocuprosis (e.g., Suttle,
1983; Mill and Davis, 1987; Underwood and Suttle,
1999). Large animal feeding operations typically keep
close watch on animal condition and diet, and would
logically address a potential Mo problem quickly with
additional Cu supplements, or alternative feeds. The
common sense and practicality of good pasture and ani-
mal management should add significant confidence to
the risk assessment presented here.
Uncertainties in the Risk Assessment
A weakness in the original USEPA risk assessment
was the limited animal (HEI) response database, espe-
cially animals consuming forages grown on biosolids-
amended land. Much of the animal response data used
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
to justify low (⬍10 mg Mo kg⫺1 ) threshold intake (TPI)
values, for example, were based on Mo salt additions
to diets of confined animals. There are very few studies
involving biosolids-Mo fertilized forage grazed by rumi-
nants (e.g., O’Connor and McDowell, 1999; K. Bro-
ersma and W.C. Gardner, personal communication,
1999). Gardner et al. (1996) recently reported minimal
responses of cattle to grazed forages with total Mo con-
centrations of 20 to 40 mg Mo kg⫺1 and forage Cu to
Mo ratios ⬍1. Forage (including legumes) was grown
on mine spoils with high pH (calcareous). Molybdenum
concentrations in animal plasma and livers increased,
but there was no evidence of molybdenosis or detrimen-
tal effects in the animals. Cattle supplemented with Cu
had the same adequate Cu in plasma and livers, and
the same overall health, as nonsupplemented cattle. For-
age S concentrations were apparently low (but normal:
苲2 g kg⫺1 ) in their study, and may have minimized
thiomolybdate (or direct cupric sulfide) formation.
Also, Loneragan et al. (1998) noted that high Mo could
decrease ruminal production of sulfide. Thus, there may
actually have been too much Mo in the forage to pro-
mote adequate sulfide, and thiomolybdate, formation
in the Gardner et al. (1996) study. Canadian researchers
(K. Broersma and W.C. Gardner, personal communica-
tion, 1999) hypothesize that forage Mo is somehow un-
available for reaction in the ruminants, an effect similar
to reduced Mo availability when forage is dried (Alla-
way, 1977). Research into the form of Mo in the forage
and the effects of increased S in the diets is underway.
Animals are being grazed on leguminous forages grown
on biosolids-amended land (K. Broersma and W.C.
Gardner, personal communication, 1999).
Forages grown on biosolids-amended soil frequently
have increased S contents (Nguyen, 1998; O’Connor
and McDowell, 1999; McBride et al., 2000). Low-main-
tenance pastures and rangelands are often underfertil-
ized, and respond well to nutrient inputs provided in
biosolids. Bahiagrass (Paspalum notatum flugge) (Ngu-
yen, 1998; O’Connor and McDowell, 1999) was espe-
cially responsive to biosolids S, and the response was
seemingly independent of biosolids source or rate of
application (1 to 8 times agronomic rate). Forage S
concentrations in all biosolids treatments reached po-
tentially problematic levels (⬎4 g kg⫺1 ). Thus, addi-
tional attention to Pathway 6 risk assessment may be
warranted aside from Mo issues. Special vigilance for
adequate Cu supplementation of animals grazing biosol-
ids-amended land to address possible biosolids S effects
may be required.
SUMMARY AND CONCLUSIONS
Recent additions to applicable databases, along with
improvements to our understanding of biosolids Mo–
soil–plant–animal interactions, allow improved Pathway
6 risk assessment for Mo-induced hypocuprosis. Forage
uptake coefficients (UC) are now available from field
studies using modern biosolids (with typical Mo concen-
trations) representing a range of plants, soil types, and
soil pH ranges. Typical diet scenario data for cattle
1505
(species most susceptible to molybdenosis) allow calcu-
lation of a diet-weighted UC factor that better repre-
sents forage Mo exposure to cattle. Recent biosolids
use data allow estimating of the fraction of animal forage
likely to be grown on biosolids-amended land (FC) and,
thus, a more reasonable estimate of possible biosolids
Mo effect on animal diets. Data from both laboratory
and field studies show that biosolids Mo is not conserved
when land-applied and that estimates of Mo leaching
(LC) are necessary to realistically assess long-term soil
Mo status.
We incorporated these various improvements into a
modified Pathway 6 algorithm as follows:
RPc ⫽ (RC/UC) ⫻ (1/FC) ⫻ (1/LC)
where RF ⫽ 9, UC ⫽ 2.25, FC ⫽ 0.2, and LC ⫽ 0.45.
This algorithm results in a cumulative biosolids Mo
application limit (RPc ) of 40 kg Mo ha⫺1 and a corre-
sponding alternate pollutant concentration (Table 3 of
Part 503) of 40 mg Mo kg⫺1. We regard our modifica-
tions and calculations as conservative, and believe the
risk of Mo toxicity from biosolids Mo is small in the
vast majority of situations. Normal good pasture and
animal management (especially, providing adequate Cu
mineral supplementation) would complement the con-
servatism of the risk assessment presented here.
ACKNOWLEDGMENTS
Many people provided invaluable input to this effort. Some,
for example, J.T. Artiola, N.T. Basta, K. Broersma, W. Gard-
ner, T.C. Granato, and M. McBride provided critical data
(unpublished at the time) for consideration. These and others
(notably J. Ryan, T.J. Logan, and R.H. Dowdy) offered in-
sightful comments to the modified algorithm development.
Too numerous to name are the many people who responded
to phone calls and emails from the senior author requesting
help to understand the system and normal agronomic and
animal management practices, nationwide. We warmly thank
all who cooperated and rightfully accept responsibility for any
misinterpretation of their input.
REFERENCES
Allaway, W.H. 1977. Perspectives on molybdenum in soils and plants.
p. 317–339. In W.R. Chappell and K.K. Petersen (ed.) Molybdenum
in the environment. Vol. 2. Marcel Dekker, New York.
Alloway, B.J. 1973. Copper and molybdenum in swayback pastures.
J. Agric. Sci. (Cambridge) 80:521–524.
Anke, M., B. Groppel, and M. Grun. 1985. Essentiality, toxicity, re-
quirement, and supply of molybdenum in humans and animals. p.
154. In C.F. Mills et al. (ed.) Trace elements in man and animals.
Commonwealth Agric. Bureaux, Farnham Royal, UK.
Barbarick, K.A., U.A. Ippolito, and D.G. Westfall. 1995. Biosolids
effects on phosphorus, copper, zinc, nickel, and molybdenum con-
centrations in dryland wheat. J. Environ. Qual. 24:608–611.
Barber, S.A. 1984. Soil nutrient bioavailability: A mechanistic ap-
proach. John Wiley & Sons, New York.
Basta, N.T., W.R. Raun, J.L. Schroder, S.B. Phillips, W.E. Thomason,
and G.V. Johnson. 1999. Effect of long-term application of biosolids
on molybdenum content of winter wheat forage. p. 348. In 1999
Agronomy abstracts. ASA, Madison, WI.
Bastain, R.K. 1997. The biosolids (sludge) treatment, beneficial use,
and disposal situation in the USA. Eur. Water Pollut. Control 7:
62–79.
Bastain, R.K., and R.B. Brobst. 1993. Molybdenum occurrence in
1506 J. ENVIRON. QUAL., VOL. 30, SEPTEMBER–OCTOBER 2001
biosolids—Sources and techniques. In Proc. of the Water Environ.
Fed. Specialty Conf., Phoenix, AZ. 4–5 Dec. 1993. Water Environ.
Fed., Phoenix, AZ.
Brinton, S.R., and G.A. O’Connor. 2000. Factors affecting molybde-
num sorption in soils: Potential biosolids effects. Proc. Soil Crop
Sci. Soc. Fla. 59:117–123.
Cameron, H.S., and H. Goss. 1948. Effect of molybdenum on livestock
in permanent pastures. Calif. Agric. 2:6.
Chang, A.C., and A.L. Page. 2000. Trace elements slowly accumulat-
ing, depleting in soils. Calif. Agric. 54:49–55.
Clawson, W.J., A.L. Lesperance, V.R. Bohman, and D.C. Layhee.
1972. Interrelationship of dietary molybdenum and copper on
growth and tissue composition of cattle. J. Anim. Sci. 34:516–520.
Dick, A.T. 1956. Molybdenum in animal nutrition. Soil Sci. 81:229–258.
Draeger, K.J., J.W. Pundsack, D.M. Jorgenson, and P.J. Malloy. 1999.
Watershed effects of biosolids application: Literature review. Proj-
ect 96-REM-2 Final Rep. Water Environ. Res. Foundation, Alex-
andria, VA.
Ensminger, M.E., J.E. Oldfield, and W.W. Heinemann. 1990. Feeding.
p. 591–1169. In Feeds and nutrition. The Ensminger Publ. Co.,
Clovis, CA.
Etgen, W.M., R.E. James, and P.M. Reaves. 1987. Feedstuffs and
management. John Wiley & Sons, New York.
Ferguson, W.S., A.H. Lewis, and S.J. Watson. 1943. The teart pastures
of Somerset: I. The cause and cure of teartness. J. Agric. Sci.
(Cambridge) 33:44–51.
Field, A. 1981. Information needs in mineral nutrition of ruminants.
p. 233–242. In Florida Nutrition Conf., St. Petersburg Beach, FL.
14 June 1981. Univ. of Florida, Gainesville.
Flynn, A., A.W. Franzman, and P.D. Arneson. 1977. Molybdenum–
sulfur interactions in the utilization of marginal dietary copper in
Alaskan moose (Alces alces gigas ). p. 115–124. In W.R. Chappell
and K.K. Petersen (ed.) Molybdenum in the environment. Vol. 1.
Marcel Dekker, New York.
Frieberg, L., P. Boston, G. Norberg, M. Piscator, and K. Robert.
1975. Molybdenum—A toxicological appraisal. EPA-600/1-75-004.
USEPA, Research Triangle Park, NC.
Gardner, W.C., J.D. Popp, D.A. Quinton, Z. Mir, and W.T. Buckley.
1996. Animal response to grazing on reclaimed mine tailings. p.
23–31. In Proc. 20th Annu. B.C. Mine Reclamation Symp., Kam-
loops, BC, Canada. 17–20 June 1996. Bitech Publ., Richmond,
BC, Canada.
Gartrell, J.W. 1981. Distribution and correction of copper deficiency
in crops and pastures. p. 313–349. In J.F. Loneragan et al. (ed.)
Copper in soils and plants. Academic Press, New York.
Georgievskii, V.I., B.N. Annenhov, and V.T. Samokhin. 1981. Mineral
nutrition of animals. Butterworths, London.
Goldberg, S., H.S. Forster, and C.L. Godfrey. 1996. Molybdenum
adsorption on oxides, clay minerals, and soils. Soil Sci. Soc. Am.
J. 60:425–432.
Goldberg, S., C. Su, and H.S. Forster. 1998. Factors affecting molybde-
num adsorption by soils and minerals. Soil Sci. 163:109–114.
Gooneratne, S.R., W.T. Buckley, and D.A. Christensen. 1989. Review
of copper deficiency and metabolism in ruminants. Can. J. Anim.
Sci. 69:819–845.
Gupta, U.C. 1997a. Molybdenum in agriculture. Cambridge Univ.
Press, Cambridge.
Gupta, U.C. 1997b. Soil and plant factors affecting molybdenum up-
take by plants. p. 71–91. In U.C. Gupta (ed.) Molybdenum in
agriculture. Cambridge Univ. Press, Cambridge.
Hemkes, O.J., A. Kemp, and L.W. Broekhoven. 1980. Accumulation
of heavy metals in the soil due to annual dressing with sewage
sludge. Neth. J. Agric. Sci. 28:228–237.
Hornick, S.B., D.E. Baker, and S.B. Guss. 1977. Crop production and
animal health problems associated with high soil molybdenum. p.
665–684. In W.R. Chappell and K.K. Petersson (ed.) Molybdenum
in the environment. Vol. 2. Marcel Dekker, New York.
Huber, J.T., N.D. Price, and R.W. Engel. 1971. Response of lactating
dairy cows to high levels of dietary molybdenum. J. Anim. Sci.
32:364–367.
International Molybdenum Association. 1999. International Molybde-
num Association [Online]. Available at http://www.imoa.org.uk/
(verified 26 Apr. 2001).
Janonis, B.A., McGaha Miller, and J.A. Billca. 1996. The results of
a biosolids demonstration project to assess operational environ-
mental impacts on rangeland. In Proc. of the Water Environ. Fed.
10th Annu. Residuals and Biosolids Manage. Conf., Denver, CO.
18–21 Aug. 1996. Water Environ. Fed., Alexandria, VA.
Johansen, D., P.C. Kerridge, and A. Sultana. 1997. Responses of
forage legumes and grasses to molybdenum. p. 208–228. In U.C.
Gupta (ed.) Molybdenum in agriculture. Cambridge Univ. Press,
Cambridge.
Kabata-Pendias, A., and H. Pendias. 1991. Trace elements in soils
and plants. 2nd ed. CRC Press, Boca Raton, FL.
Kandylis, K. 1984. Toxicology of sulfur in ruminants: A review. J.
Dairy Sci. 67:2179–2187.
Kincaid, R.L., R.M. Blauwiekel, and J.D. Cronrath. 1986. Supplemen-
tation of copper as copper sulfate or copper proteinate for growing
calves fed forages containing molybdenum. J. Dairy Sci. 69:160–163.
Kubota, J. 1974. Mineral composition of browse plants for moose
(soil–plant–animal relationships). Le Naturaliste Can. 101:291–305.
Kubota, J. 1977. Molybdenum status of United States soils and plants.
p. 555–581. In W.R. Chappell and K.K. Petersen (ed.) Molybdenum
in the environment. Vol 2. Marcel Dekker, New York.
Kubota, J., V.A. Lazar, L.N. Langan, and K.C. Beeson. 1961. The
relationship of soils to molybdenum toxicity in cattle in Nevada.
Soil Sci. Soc. Am. Proc. 25:227–232.
Kubota, J., E.R. Lemon, and W.H. Allaway. 1963. The effect of soil
moisture content upon the uptake of molybdenum, copper, and
cobalt by Aliske clover. Soil Sci. Soc. Am. Proc. 27:679–683.
Lewis, A.H. 1943. The teart pastures of Somerset: III. Reducing the
teartness of pasture herbage. J. Agric. Sci. (Cambridge) 33:58–63.
Logan, T.J. 1997. Balancing benefits and risks in biosolids. Biocycle
38:52–57.
Loneragan, G.H., D.H. Gould, and F.B. Garry. 1998. Field investiga-
tions of sulfur-associated polioencephalomalacia (PEM). J. Anim.
Sci. 76(Suppl. 1):361.
Mason, J. 1986. Thiomolybdates: Mediators of molybdenum toxicity
and enzyme inhibitors. Toxicology 42:99–109.
Mason, J. 1990. The biochemical pathogenesis of molybdenum-in-
duced copper deficiency syndromes in ruminants: Toward the final
chapter. Irish Vet. J. 43:18–21.
McBride, M.B. 1998. Soluble trace metals in alkaline stabilized sludge
products. J. Environ. Qual. 27:578–584.
McBride, M.B., B.K. Richards, T. Steenhuis, and G. Spiers. 1999.
Long-term leaching of trace elements in a heavily sludge-amended
silty clay loam soil. Soil Sci. 164:613–623.
McBride, M.B., B.K. Richards, T. Steenhuis, and G. Spiers. 2000.
Molybdenum uptake by forage crops grown on sewage sludge-
amended soils in the field and greenhouse. J. Environ. Qual. 29:
848–854.
McCurry, G.N. 1995. Evaluating infiltration-related water quality im-
pcats associated with land application of biosolids in arid and semi-
arid settings. p. 4-1 through 4-22. In Proc. Effects of Land Applica-
tion of Biosolids in Arid and Semi-Arid Environ., Fort Collins,
CO. 16–19 May 1995. Doc. 908-B-95-001. USEPA, Denver, CO.
McDowell, L.R. 1992. Minerals in animal and human nutrition. Aca-
demic Press, San Diego, CA.
McDowell, L.R. 1997. Minerals for grazing ruminants in tropical re-
gions. Ext. Bull. Dep. Animal Sci., Center for Tropical Agric.,
Univ. of Florida, Gainesville.
Michalk, D.L. 1995. Evaluation of sewage sludge products for use in
extensive sheep production systems in Australia. In Proc. Effects
of Land Application of Biosolids in Arid and Semi-Arid Environ.,
Fort Collins, CO. 16–19 May 1995. Doc. 908-B-95-001. USEPA,
Denver, CO.
Mills, D.F., and G.K. Davis. 1987. Molybdenum. p. 429–465. In W.
Mertz (ed.) Trace elements in human and animal nutrition. Vol.
1. Academic Press, New York.
Miltimore, J.E., and J.L. Mason. 1971. Copper to molybdenum ratio
and molybdenum and copper concentrations in ruminant feeds.
Can. J. Anim. Sci. 51:193–200.
Moffet, C., R. Zartman, C. Brenton, E. Fish, D. Webster, and R. Sose-
bee. 1995. Municipal biosolids application effects on infiltration
and erosion on desert grasslands. p. 4-23 through 4-45. In Proc.
Effects of Land Application of Biosolids in Arid and Semi-Arid
Environ., Fort Collins, CO. 16–19 May 1995. Doc. 908-B-95-001.
USEPA, Denver, CO.
 O’CONNOR ET AL.: MO STANDARDS FOR LAND APPLICATION OF BIOSOLIDS
Mowrey, A., and J.N. Spain. 1999. Results of a nationwide survey to
determine feedstuffs fed to lactating dairy cows. J. Dairy Sci. 82:
445–451.
National Research Council. 1980. Mineral tolerance of domestic ani-
mals. National Academy Press, Washington, DC.
National Research Council. 1996. Use of reclaimed water and sludge
in food production. National Academy Press, Washington, DC.
Nguyen, H.Q. 1998. Bahiagrass (Paspalum notatum flugge ) response
to anaerobically digested pelletized biosolids. M.S. thesis. Univ. of
Florida, Gainesville.
O’Connor, G.A., T.C. Granato, and N.T. Basta. 2001a. Bioavailability
of biosolids molybdenum to soybean grain. J. Environ. Qual. 30:
1653–1658 (this issue).
O’Connor, G.A., T.C. Granato, and R.H. Dowdy. 2001b. Bioavailabil-
ity of biosolids molybdenum to corn. J. Environ. Qual. 30:140–146.
O’Connor, G.A., and L.R. McDowell. 1999. Understanding fate, trans-
port, bioavailability, and cycling of metals in land-applied biosolids.
Project 95-REM-3 Final Rep. Water Environ. Res. Foundation,
Alexandria, VA.
Phillippo, M., W.R. Humphries, T. Atkinson, G.D. Henderson, and
P.H. Garthwaite. 1987. The effect of dietary molybdenum and iron
on copper status, puberty, fertility and oestrous cycles in cattle. J.
Agric. Sci. (Cambridge) 109:321–336.
Phillips, R.L., and R.D. Meyer. 1993. Molybdenum concentrations of
alfalfa in Kern County California: 1950 versus 1985. Commun. Soil
Sci. Plant Anal. 24:2725–2731.
Pierzynski, G.M., and L.W. Jacobs. 1986. Molybdenum accumulation
by corn and soybeans from a molybdenum-rich sewage sludge. J.
Environ. Qual. 15:394–398.
Ryan, J., M. McKillen, and J. Mason. 1987. Sulphate/molybdate inter-
actions: In vivo and in vitro studies on the group VI oxyanion
transport system in ovine renal tubule epithelial cells. Ann. Rech.
Vet. 18:47–55.
Soon, Y.K., and T.E. Bates. 1985. Molybdenum, cobalt, and boron
uptake from sewage sludge amended soils. Can. J. Soil Sci. 65:
507–517.
Suttle, N.F. 1973. Effects of age and weaning on the apparent availabil-
ity of dietary copper to young lambs. Proc. Nutr. Soc. 32:24A–25A.
Suttle, N.F. 1980. Some preliminary observations on the absorbability
of copper in fresh and conserved grass to sheep. Proc. Nutr. Soc.
39:63A.
Suttle, N.F. 1983. Effects of molybdenum concentration in fresh herb-
age, hay and semi-purified diets on the copper metabolism of sheep.
J. Agric. Sci. (Cambridge) 100:651–656.
Suttle, N.F. 1986. Problems in the diagnosis and anticipation of trace
element deficiencies in grazing livestock. Vet Record 119:148–152.
Suttle, N.F. 1991. The interactions between copper, molybdenum, and
sulfur in ruminant nutrition. Annu. Rev. Nutr. 11:121–140.
Suttle, N.F., P. Abrahams, and I. Thorton. 1984. The role of a soil ⫻
dietary sulfur interaction in the impairment of copper absorption
by ingested soil in sheep. J. Agric. Sci. (Cambridge) 103:81–86.
1507
Suttle, N.F., B.J. Alloway, and I. Thorton. 1975. An effect of soil
ingestion on the utilization of dietary copper by sheep. J. Agric.
Sci. (Cambridge) 84:249–254.
Underwood, E.J. 1981. The mineral nutrition of livestock. 2nd ed.
CAB Int., Farnham Royal, UK.
Underwood, E.J., and N.F. Suttle. 1999. The mineral nutrition of
livestock. 3rd ed. CAB Int., Farnham Royal, UK.
USDA. 1999. 1997 census of agriculture. USDA Natl. Agric. Stat.
Serv., Washington, DC.
USEPA. 1988. Proposed prohibition of hexavalent chromium chemi-
cals in cooling towers: Proposed Rule. 40 CFR Part 749. Fed.
Regist. 53:10 206–10 221.
USEPA. 1989. Risk of unsaturated/saturated transport and transfor-
mation of chemical concentrations (RUSTIC), Vol. II: User’s guide.
EPA/600/3-89/048b. Environ. Res. Lab., Athens, GA.
USEPA. 1990a. Prohibition of hexavalent chromium chemicals in
comfort cooling towers: Final Rule. 40 CFR Part 749. Fed. Regist.
55:222–241.
USEPA. 1990b. National sewage sludge survey: Availability of infor-
mation and data, and anticipated impacts on proposed rule 40 CFR
Part 503. Fed. Regist. 55:47 210–47 283.
USEPA. 1992. Technical support document for land application of
sewage sludge. NTIS PB93-110575. Office of Water, Springfield, VA.
USEPA. 1994. 40 CFR Part 503—Standards for the use or disposal
of sewage sludge: Final rule. Fed. Regist. 59:9095–9100.
Vlek, P.L.G., and W.L. Lindsay. 1977. Molybdenum contamination
in Colorado pasture soils. p. 619–650. In W.R. Chappell and K.K.
Petersen (ed.) Molybdenum in the environment. Vol. 2. Marcel Dek-
ker, New York.
Ward, G.M. 1994. Molybdenum requirements, toxicity and nutritional
limits for man and animals. p. 452–476. In E.R. Braithwaite and
J. Haber (ed.) Molybdenum: An outline of its chemistry and use.
Studies in Inorganic Chem. 19. Elsevier, Amsterdam.
Ward, G.M., and J. Nagy. 1977. Molybdenum and copper in Colorado
forages, molybdenum toxicity in deer and copper supplementation
of cattle. p. 97–113. In W.R. Chappell and K.K. Peterson (ed.)
Molybdenum in the environment. Vol. 1. Marcel Dekker, New
York.
Wiener, G., and A.C. Field. 1969. Copper concentrations in the liver
and blood of sheep of different breeds in relation to swayback
history. J. Comp. Pathol. 79:7–14.
Williams, J.H., and J.C. Gogna. 1981. Molybdenum uptake from sew-
age sludge treated soil. p. 189–193. In Proc. Int. Conf. Heavy Metals
in the Environ., Amsterdam. 15–18 Sept. 1981. CEP Consultants, Ed-
inburgh.
Yeh, G.T. 1981. AT123D: Analytical transport one-, two-, and three-
dimensional simulation of waste transport in the aquifer system.
Environ. Serv. Div. Publ. no. 1439. Oak Ridge National Lab., Oak
Ridge, TN.