Chemosphere 61 (2005) 85–91

www.elsevier.com/locate/chemosphere

Transport and fate of dieldrin in poplar and willowtrees analyzed by SPME

Serena V. Skaates a, Anu Ramaswami b,*, Larry G. Anderson a

a Department of Chemistry, University of Colorado at Denver, Denver, CO 80202, USAb Department of Civil Engineering, University of Colorado at Denver, P.O. Box 173364, Denver, CO 80202, USA

Received 13 July 2004; received in revised form 2 March 2005; accepted 7 March 2005

Available online 12 May 2005

Abstract

Dieldrin is a hydrophobic organochlorine insecticide that is persistent in the environment. The fate and transport of

dieldrin in trees is important both in the context of potential remediation, as well as food chain impacts through dieldrin

transport to shoots and leaves. Experiments were conducted to measure the degree of dieldrin partitioning to plant tis-

sue and the potential for biodegradation of dieldrin in the microbe rich tree rhizosphere. Dieldrin was analyzed in water

and plant tissue using headspace solid-phase microextraction (SPME) coupled with gas chromatography. Poplar and

willow saplings planted in soil and watered with 10 lg l�1 dieldrin for up to 9 months showed no adverse effects due

to dieldrin exposure and no dieldrin was observed in plant shoots with a method detection limit (MDL) of 7 ng g�1.

One-week hydroponic tests of poplar saplings exposed to aqueous dieldrin also showed no detection of dieldrin in

shoots, with an average of 66% of the dieldrin partitioned to the plant roots and an overall mass balance recovery

of 76% in the plant–water system. The root concentration factor (RCF) was found to be 30 ± 3 ml water g�1 root. Bio-

degradation of dieldrin was not observed in an aqueous batch bioreactor containing 8 lg l�1 dieldrin, nutrients and bac-

teria from the root zone of a poplar sapling that had been exposed to dieldrin for 9 months. These results show that

planting trees is likely to be safe and potentially useful at sites containing low-levels of dieldrin in groundwater.

� 2005 Published by Elsevier Ltd.

Keywords: Phytoremediation; Solid-phase microextraction; Root concentration factor; Biodegradation

1. Introduction

Dieldrin (Fig. 1) is a polychlorinated Diels–Alder ad-

duct that was first manufactured in the 1950s for use as

an insecticide (IPCS, 1989). It has been banned for use in

several countries since the early 1970s because of acutely

0045-6535/$ - see front matter � 2005 Published by Elsevier Ltd.

doi:10.1016/j.chemosphere.2005.03.014

* Corresponding author. Tel.: +1 303 556 4734; fax: +1 303

556 2368.

E-mail address: aramaswa@carbon.cudenver.edu (A. Rama-

swami).

toxic, mutagenic and teratogenic effects on mammals

(ATSDR, 2002). Dieldrin exhibits very low water solu-

bility, sorbs strongly to organic matter in the subsurface

and exhibits limited partitioning to air. The latter prop-

erties of dieldrin are characterized by an octanol–water

partition coefficient (Kow) of 2.5 · 105 l water l octanol�1

(Lyman, 1990) and an air–water partition coefficient of

4.5 · 10�5 l water l air�1 (Mackay et al., 1992). Ground-

water at the Rocky Mountain Arsenal (RMA) site near

Denver, CO, contains dieldrin at sub-ppb levels along

with several other organic contaminants, such as chloro-

form and diisopropyl methylphosphonate (ATSDR,

Fig. 1. Chemical structure of dieldrin.

86 S.V. Skaates et al. / Chemosphere 61 (2005) 85–91

1996). The Containment System Remediation Goal for

dieldrin is 0.002 lg l�1 with a Practical Quantitation

Limit of 0.05 lg l�1 (FWEC, 1996). Low-cost remedia-

tion technologies such as phytoremediation are being

evaluated for enhancement to the existing pump and

treat systems for groundwater remediation at the

RMA site.

The uptake of dieldrin by trees can be quantified in

part by the root concentration factor (RCF), which is

defined as the ratio of chemical concentration in roots

to that in the surrounding waters. Highly hydrophobic

contaminants such as dieldrin have been shown to parti-

tion preferentially to the root tissue rather than entering

the transpiration stream (Briggs et al., 1982; Burken and

Schnoor, 1998). Using RCF-Kow correlations previously

determined for a set of 12 chemicals (Burken and Sch-

noor, 1997), the RCF for dieldrin in poplar trees is esti-

mated to be 90 ml water/g root. However, the estimated

RCF needs to be supported with experimental data since

the behavior of dieldrin may differ from that of the com-

pounds from which the correlations were derived. No

study to date has measured plant-partitioning parame-

ters for dieldrin.

The plant rhizosphere is the soil region influenced by

plant roots to support enhanced microbial growth.

Microorganisms feed on root exudates and epidermal

cells resulting in an order of magnitude more bacteria

in the rhizosphere as compared to bulk soil (Anderson

et al., 1993). Although dieldrin is known to be persistent

in the environment, Matsumura and Boush (1967) found

evidence for biodegradation of dieldrin in soil samples

from several contaminated sites, including the Rocky

Mountain Arsenal. In a more recent study, Hugenholts

and MacRae (1990) observed biodegradation of dieldrin

only with the addition of organic soil amendments

which are thought to act as growth substrates. No infor-

mation is currently available on dieldrin degradation in

the rhizosphere of plants.

Both poplar and willow trees are being considered for

phytoremediation applications at RMA, and hence

small saplings of these plants were used in four types

of laboratory tests to evaluate transport and fate of diel-

drin in trees. (1) A long-term exposure test in which soil-

planted saplings were watered for several months with

dieldrin to evaluate potential for above-ground translo-

cation of dieldrin. (2) A hydroponic test during which

poplar saplings were placed in aqueous dieldrin for

1 week to assess a mass balance of dieldrin in the

plant–water system. (3) An RCF test with exposure of

cut poplar roots to dieldrin in water. (4) A biodegrada-

tion test to determine if microbial degradation of diel-

drin could be observed based on loss of mass from an

aqueous bioreactor system containing rhizosphere bac-

teria, nutrients and dieldrin. Dieldrin analysis in all tests

was accomplished using a relatively new, solventless,

eco-friendly microfiber extraction technique (Zhang

and Pawliszyn, 1993). The efficacy of this analytical

technique is also described in this paper.

2. Experimental methods

2.1. Long-term exposure

Two weeping willow cuttings were planted in 2-L

glass jars without drainage. The soil was prepared by

mixing two parts sand with one part topsoil, by volume,

for an organic matter content of 0.7%, which is close to

the organic matter content of the soil at the contami-

nated site (0.5%).

The trees were irrigated with 225 ml on average per

week of 10 lg l�1 dieldrin solution through glass tubing

inserted to the bottom of the glass jar for 7 and

9 months. At the end of the test period, plants were

removed from the soil and the roots were rinsed to dis-

lodge attached soil particles. The plant tissue was

processed for analysis as described below for the hydro-

ponic test.

2.2. Hydroponic test

Hybrid poplar (Populus deltoids · nigra) saplings

were obtained from the Colorado State Forest Service

as bare root cuttings 1–2 cm in diameter and 90 cm long.

The cuttings were inserted through the septum of 200 ml

septa jar lids (I-Chem) and allowed to bud out in green-

house conditions such that the shoots and roots devel-

oped above and below the lids, respectively.

The poplar saplings, grown in this manner, were ex-

posed to dieldrin by fitting the plant-inserted jar lids

onto glass jars that contained 200 ml of 10 lg l�1 aque-

ous dieldrin solutions. The dieldrin solution was pre-

pared by diluting a 20-lg ml�1 standard solution of

dieldrin in methanol (Supelco). Three planted systems

were prepared in this manner and exposed to dieldrin.

An additional sapling was cut off just above the roots,

which were exposed to aqueous dieldrin, and is referred

to as the severed root. Two additional saplings served as

S.V. Skaates et al. / Chemosphere 61 (2005) 85–91 87

the unexposed control plants. One jar containing 10-

lg l�1 aqueous dieldrin was capped without a plant

and served as the unplanted control.

The dieldrin-exposed plants, the unplanted control

jar and the unexposed control plants were placed inside

a sunny window for 7 days. All jars were covered with

aluminum foil to prevent potential photodegradation

of dieldrin. Water loss by evaporation/transpiration

was monitored by tracking mass loss in the jar system.

At the end of the test period, the plant roots and shoots

were separated, blended in liquid nitrogen and stored

frozen prior to analysis. The solution in the jars were

reconstituted to their original volume with tap water

to gather any dieldrin residue on the glass surface and

refrigerated until analysis.

2.3. RCF test

In the hydroponic exposure test, there was significant

variation in the amount of water transpired by each

sample. The differing degrees of surface contact affected

physical sorption of dieldrin to the roots. Therefore, the

RCF test was performed in triplicate with 10 g roots sev-

ered from the stem and submerged in approximately

200 ml of 10-lg l�1 dieldrin. Three replicates were pre-

pared in this manner. Another 10-g root sample was

contacted with water to serve as the unexposed control.

The jars were sealed with Teflon-lined screw caps and

left in a dark place for 13 days. The solution from one

of the exposed root samples was analyzed periodically

over 1 week to determine that equilibrium had been at-

tained between water and root tissue at which time the

aqueous solution was withdrawn and stored at 4 �Cwhile the roots were processed as in the hydroponic test

for analysis. Each water and root sample was analyzed

twice, with the average value reported here.

2.4. Batch bioreactor test

An aqueous slurry batch bioreactor test was

conducted to assess whether microbes living in the

rhizosphere of the 9-month exposure sapling would

breakdown dieldrin. The experiment was set-up in the

aqueous phase to maximize the amount of soluble, and

thus bioavailable, dieldrin and to avoid large uncertain-

ties in the mass balance due to uneven distributrion of

dieldrin in soil (Ramaswami et al., 2003).

Microbes obtained from the rhizosphere of a willow

tree irrigated with dieldrin were placed in a batch biore-

actor supplied with nutrients and oxygen and evaluated

over a 2-month period for degradation of dieldrin. To

obtain rhizosphere microbes, a portion of soil from the

root zone of the 9-month exposure willow containing

thin root hairs was homogenized, and 6-g aliquots were

placed in each of five sterile polypropylene tubes. The

volume of each tube was brought to 35 ml with 10%

glucophosphate surfactant solution and shaken for 2 h.

Ten millilitres of the supernatant containing detached

microbes was added into each batch bioreactor which

contained 97 ml of 10 lg l�1 dieldrin solution, 3 ml of

1104 mg l�1 calcium chloride and 25 ml of high biologi-

cal oxygen demand (HBOD) nutrient media yielding an

initial dieldrin concentration of 7.8 lg l�1. No attempt

was made to remove fine soil particles from the superna-

tant. The HBOD nutrient media contained 0.25 mg l�1

of FeCl3 * 6H2O, 850.0 mg l�1 of NH4Cl, 170.0 mg l�1

of KH2PO4, 435.0 mg l�1 of K2HPO4, 22.5 mg l�1 of

MgSO4 * 7H2O and 608.0 mg l�1 of Na2HPO4. Five

reactors were prepared in this manner. Two of the five

were maintained as kill-controls with 1 ml of 36 g l�1

mercuric (II) chloride added to kill the microbes while

1 ml of sterile, distilled water was added to the remain-

ing three bioactive reactors for consistency. The head-

space in the jars was purged with pure oxygen every

2 days and 0.01 g poplar root hairs, unexposed to diel-

drin, were added to each sample after 5 days as an addi-

tional carbon source to stimulate co-metabolism. The

bioreactor solutions were mixed and aqueous samples

from each bioreactor were analyzed for dieldrin period-

ically for 58 days.

In order to verify the viability of the bacteria in the bio-

reactors, aqueous phase samples were withdrawn from

one kill-control reactor and from one bioactive reactor

at day 26, stained with 0.2% acridine orange, and viewed

by microscope according to the method of Hobbie et al.

(1977). The mercury-killed bioreactor sample contained

few bacteria, 90% of which were not actively growing.

In contrast, the live bioreactor sample contained an abun-

dance of bacteria that were 90% active.

3. Analytical methods

3.1. Review of SPME methods

Solid-phase microextraction (SPME) is a new extrac-

tion technique based on partition theory (Hermens et al.,

2003) during which the sample is exposed to a microfiber

coated with a non-polar polymeric phase. The extent to

which the analyte partitions to the fiber coating is pro-

portional to concentration. Following extraction, the

analyte is desorbed from the fiber directly in the heated

injection port of a gas chromatograph. SPME was used

because it requires no solvent, making it a safe and envi-

ronmentally friendly technique.

The application of SPME for measurement of orga-

nochlorine pesticides in environmental matrices is still

being explored. Table 1 compares reports of techniques

and efficiencies for SPME of dieldrin in various matri-

ces. Page and Lacroix (1997) employed headspace

extraction because they found it less susceptible to inter-

ference from impurities than immersion extraction for

Table 1

Survey of SPME analysis of dieldrin

Matrix Extraction technique GC detection Extraction

efficiency (%)

Detection

limit

RSD

(%)

Reference

Water (aldrin) Headspace 87 �C 60

min 15 ml water

Electrolytic

conductivity

45 0.004 lg l�1 8.8 Page and Lacroix (1997)

Soil Headspace 70 �C 60

min 0.5 g + 5 ml water

Electron capture Not given 0.07 ng g�1 6.6 Doong and Liao (2001)

Plant tissue Immersion room

temperature 90 min

1 g + 30 ml water

Mass spectrometry

selected ion monitoring

16.5 0.05 ng g�1 7 Hwang and Lee (2000)

88 S.V. Skaates et al. / Chemosphere 61 (2005) 85–91

aqueous samples. Doong and Liao (2001) and Hwang

and Lee (2000) were able to efficiently analyze trace lev-

els of organochlorine pesticides from low-organic matter

content soils and plant tissue, respectively, using head-

space-SPME with the addition of water to the sample.

Very few studies have demonstrated SPME methods

for dieldrin analysis in plant matrices. This paper reports

SPME methods effective for the coupled plant–water

systems studied in this project.

3.2. SPME methods

Heated headspace dieldrin extractions were per-

formed with a 1-cm, 100-lm PDMS fiber with manual

holder obtained from Supelco. Each fiber was condi-

tioned at 260 �C for 30 min inside the GC injection port

prior to its first use, and for 5 min before the first extrac-

tion in a sequence. Aqueous samples and calibration

standards were contained in glass vials with PTFE-lined

septum caps and PTFE-coated stir-bars and placed on a

heat/stir plate. Biomass samples and calibration stan-

dards were placed in water in glass vials and also under-

went headspace extraction. The samples were allowed to

heat for 6 min on the plate before the fiber was inserted

into the vortex of the stirred sample. Immediately fol-

lowing each extraction, the fiber was placed in the

heated GC injection port for 5 min.

For aqueous solutions, 3 ml of sample in a 4 ml vial

was heated with stirring to 70 ± 2 �C. The fiber was

exposed to the headspace for 50 min. For plant tissue

analysis, 1 g of frozen, blended tree roots or shoots were

placed in a 10-ml vial with 6 ml of water. The sample

was stirred and heated to 85 ± 2 �C and the fiber was

exposed to the headspace for 30 min.

Clean water calibration standards for the long-term

and hydroponic exposure tests were prepared by appro-

priately diluting a 20 mg l�1 dieldrin in methanol stan-

dard solution (Supelco), first in acetonitrile, then in

water. The highest calibration standard at 50 lg l�1

was made from direct dilution of the 20 mg l�1 standard.

Solvent composition of calibration standards was 1.3%

or less.

Separate calibration curves were used for the analysis

of clean versus root-exposed aqueous samples because

of the natural organic matter in the latter. Root-exposed

water calibration standards were prepared for the ana-

lysis of these samples by adding appropriate amounts

of a 10 lg l�1 dieldrin in tap water solution to aliquots

of the root exposed tap water control from the RCF test.

One millilitre of 0.0113 N sodium thiosulfate (Hach) per

40 ml for a final concentration of 0.3 mN was included

in all aqueous calibration standards to scavenge chlorine

ions.

Calibration standards for the plant tissue matrix were

generated by adding 6 ml of aqueous diedrin standard

solutions onto 1 g of unexposed d. nigra plant tissue

and equilibrating at room temperature for at least 3 h

prior to analysis. The plant tissue spike solutions were

prepared by appropriately diluting 50-lg l�1 dieldrin in

tap water.

Although several variations on the SPME method

were tried based on literature reports (see Table 1),

including immersing the fiber in a slurry of water and

blended plant tissue according to the method of Hwang

and Lee (2000), headspace-SPME, as described above,

proved to be the most effective with an average extrac-

tion efficiency of 1%.

3.3. Gas chromatograph

Separations were performed in splitless mode on an

SRI 8610c gas chromatograph with a dry electrolytic

conductivity detector (DELCD) using a Restek 60 m ·0.53 mm · 0.5 lm MXT-1 column and a 0.75 mm ID

glass injection sleeve (Supelco) designed for SPME. The

injection port temperature was 260 �C and helium was

used as the carrier gas. The oven was initially held at

120 �C for 2 min, raised by 30 �C/min–180 �C then

ramped at 10 �C/min–260 �C and held for 15 min.

3.4. Calibration

Sample concentrations were determined by compari-

son to matrix spike calibration curves processed by

Table 2

SPME calibration data for quantitation of dieldrin in various matrices

Curve n Extraction

efficiency %

Fit R2 % RSD Range IDL

Clean water 19 55 Linear 0.993 7 (n = 5 at 7.8 lg l�1) 0.2–50 lg l�1 0.1 mg l�1

Root-exposed water 9 43 Linear 0.975 15 (n = 3 at 0.2 lg l�1) 0.2–2.3 lg l�1 0.1 ml l�1

Roots 33 1 Quadratic 0.901 14 (n = 13 at 100 ng g�1) 10–300 ng g�1 <10 ng g�1

Shoots 15 1 Quadratic 0.998 21 (n = 6 at 10 ng g�1) 2–300 ng g�1 <10 ng g�1

S.V. Skaates et al. / Chemosphere 61 (2005) 85–91 89

SPME. Comprehensive calibration curve data is shown

in Table 2. The 55% extraction efficiency from the clean

aqueous matrix is comparative to the 45% efficiency re-

ported by Page and Lacroix (1997) for heated-headspace

SPME of aldrin, a derivative of dieldrin (see Table 1).

The instrumental detection limit (IDL) is based on a

signal-to-noise ratio of at least 3, whereas the method

detection limit (MDL) was determined by signal-

to-noise and variance, according to the US EPA MDL

procedure (EPA, 1997).

Aqueous and root-exposed tap water blanks yielded

a small signal due to desorption of dieldrin from the

PTFE-coated stir bars previously exposed to dieldrin

during SPME, despite multiple washes with solvent.

This desorption also caused greater variation in

response at low concentrations (<1 lg l�1).

4. Experimental results

4.1. Long-term exposure test

No ill-effects were observed in saplings exposed to

10 lg l�1 dieldrin compared to unexposed plants. Diel-

drin was found in the roots of the seven-month exposed

willow at a concentration of 26 ng g�1 and at 16 ng g�1

in the 9-month exposed willow. Dieldrin was not

detected in the shoots of either plant.

4.2. Hydroponic test

Results from the hydroponic tests verified the general

expectation that dieldrin partitions strongly to root

Table 3

Results of the hydroponic exposure of poplar saplings to dieldrin

Dieldrin hydroponic test Plan

Initial volume ml 202

Initial dieldrin concentration in water ng l�1 9

Volume evapo-transpired ml 195.

Final dieldrin concentration in reconstituted water ng l�1 1.1

Mass of roots g 14.1

Dieldrin concentration in roots ng g�1 80

Dieldrin concentration in shoot ng g�1 bdl

Dieldrin mass recovered % 69

bdl = Below detection limit.

material. The final dieldrin concentration in the un-

planted control jar matched the initial, measured value.

Each root-exposed water and plant tissue sample in the

hydroponic test was analyzed in duplicate with the aver-

ages reported in Table 3. Dieldrin was not detected in

the shoots of any of the exposed saplings with an

MDL of 7 ng g�1.

Fig. 2a and b show the distribution of dieldrin in the

planted systems and the severed root, respectively, with

the bulk of the mass in the roots. The mass distribution

of dieldrin in water and in roots is similar with and with-

out the aerial portion of the plants, which indicates that

the apparent incomplete mass recovery is attributable to

the propagation of analytical error in the coupled water–

biomass system (see Table 2) and not related to translo-

cation to shoots (bdl).

4.3. RCF test

The RCF was computed as the ratio of the final con-

centration of dieldrin in cut poplar roots to the time-

averaged initial and final concentration of dieldrin

in water for a value of 30 ± 3 ml water g root�1. The

time-averaged aqueous dieldrin concentration in the

denominator represents the average concentration

the tree is exposed to over the course of the experi-

ment (Burken and Schnoor, 1997). Results for the

RCF test are given as the average of three samples in

Table 4.

The RCF test mass balance is shown in Fig. 3. As

with the severed root, comparing the RCF test with sap-

lings in the hydroponic test shows that the mass distribu-

tion of aqueous dieldrin and roots in a closed system is

t 1 Plant 2 Plant 3 Plant average Severed root

205.3 211.9 206 217.9

9 9 9 9

2 204.7 60.7 150 14.2

0.7 1.1 0.9 0.9

19.1 28.1 20.4 19.8

70 50 70 70

bdl bdl – –

79 79 76 78

Planted Systems 1-3

66%10%

24%

roots

water

unknown

Severed Root

69%

9%

22%

roots

water

unknown

(a) (b)

Fig. 2. Dieldrin mass distribution in the open plant–water hydroponic system (a) Plants 1–3, (b) severed root.

Table 4

Results of the RCF test

RCF test n = 3 Average Standard deviation

Aqueous volume ml 202 2

Initial dieldrin concentration in water ng l�1 10.1 –

Final dieldrin concentration in water ng l�1 0.4 0.1

Dieldrin concentration in roots ng g�1 160 10

Root concentration factor (RCF) 30 3

Dieldrin mass recovered % 80 7

RCF Test

76%

4%

20%

root

water

unknown

Fig. 3. Dieldrin mass distribution in the closed root–water

exposure test.

90 S.V. Skaates et al. / Chemosphere 61 (2005) 85–91

similar to the mass distribution values for transpiring

hydroponic plants. The slightly greater degree of diel-

drin root uptake in the RCF test is due to greater surface

contact of the cut, submerged roots.

4.4. Batch bioreactor test

The dieldrin concentration in the live bioreactors did

not decrease significantly compared to the kill-control

bioreactors (data not shown). Therefore no evidence

was found for the biodegradation of 10 lg l�1 dieldrin

over 2 months, even with microbes acclimated to diel-

drin in the plant rhizosphere for 9 months.

A higher dieldrin concentration and a different con-

sortium of microbes (Matsumura and Boush, 1967)

may yield different results.

5. Discussion

SPME was explored as a method to determine the

fate and transport of dieldrin in plant systems. SPME

was effective for analysis of dieldrin in water, with 55%

extraction efficiency, 7% RSD and an instrumental

detection limit of 0.1 ng l�1. For plant tissue analysis,

competition of plant matter with the microfiber for diel-

drin greatly reduced the signal, resulting in higher RSD

(14%) and a method detection limit of 7 ng g�1. For

analysis below this level, a better method is needed for

transferring hydrophobic compounds from organic

matter to the fiber coating. Combining either micro-

wave-assisted extraction, or some aspects of traditional

solvent-extraction with SPME may yield a method with

S.V. Skaates et al. / Chemosphere 61 (2005) 85–91 91

both low detection and increased resource efficiency.

However, heated headspace-SPME is simple and effec-

tive in determining the fate and transport of dieldrin at

the 10 ng g�1 level and above.

The long-term exposure test confirmed the uptake

of dieldrin in plant roots after 7- and 9-months expo-

sure and demonstrated no measured movement of diel-

drin into above-ground shoots over the same period

(MDL = 7 ng g�1).

The hydroponic test showed that poplar sapling roots

adsorbed 66% of aqueous dieldrin over 1 week with no

detection of dieldrin in the exposed shoots.

The RCF of dieldrin in poplar roots was measured to

be 30 ± 3 l water g root�1 which is lower than Burken

and Schnoor�s estimated value of 90 (1997). However,

considering that the hydrophobicity of dieldrin is above

the range of the compounds used to form the model, a

factor of 3 difference is not unexpected.

The dieldrin mass distribution and mass recovery in

the water–biomass system is similar in the open, whole

plant hydroponic test and the closed-jar severed root

exposure test, with most of the dieldrin found in plant

roots. This observation in conjunction with non-detec-

tion of dieldrin in the shoots of the hydroponically

exposed plants provide strong evidence that the transpi-

ration stream does not contribute appreciably to above-

ground translocation of dieldrin in plants.

Batch bioreactor experiments do not provide evi-

dence for the biodegradation of 10 lg l�1 dieldrin by

the rhizosphere microbes isolated from the trees tested

in this study. Higher dieldrin concentrations, as used

in the study by Matsumura and Boush (1967), may be

required to drive bacterial consumption of the pesticide.

Acknowledgments

This project was funded by theUnited States Environ-

mental Protection Agency, (USEPA) Region 8. The con-

tents of this paper donot necessarily represent the opinion

of theUSEPARegion 8 and theRockyMountainArsenal

RemediationVentureOffice. The authors thankDr.Don-

ald Zapien of theUniversity of Colorado andDr.William

T. Foreman of the United Stated Geological Survey for

critical evaluation and discussion as well as Jeff Boone

and Ed Moss of the University of Colorado and Jesse

Kiernan of the EPA for instrumental support.

References

Agency for Toxic Substances and Disease Registry (ATSDR),

1996. Public Health Assessment, Rocky Mountain Arsenal,

Adams County, Department of Health and Human Ser-

vices, Public Health Service, Colorado. Atlanta, GA, US.

Agency for Toxic Substances and Disease Registry (ATSDR),

2002. Toxicological Profile for Aldrin and Dieldrin, Depart-

ment of Health and Human Services, Public Health Service,

Atlanta, GA, USA.

Anderson, T.A., Guthrie, E.A., Walton, B.T., 1993. Bioreme-

diation in the rhizosphere. Environ. Sci. Technol. 27 (13),

2630–2636.

Briggs, G.G., Bromilow, R.H., Evans, A., 1982. Relationship

between lipophilicity and root uptake and translocation of

non-ionized chemicals by barley. Pestic. Sci. 13, 495–504.

Burken, J.G., Schnoor, J.L., 1997. Uptake and metabolism of

atrazine by poplar trees. Environ. Sci. Technol. 31 (5),

1399–1406.

Burken, J.G., Schnoor, J.L., 1998. Predictive relationships for

uptake of organic contaminants by hybrid poplar trees.

Environ. Sci. Technol. 32 (21), 3379–3385.

Doong, R.-A., Liao, R.-L., 2001. Determination of organo-

chlorine pesticides and their metabolites in soil samples

using headspace solid-phase microextraction. J. Chroma-

togr. A 918, 177–188.

Environmental Protection Agency (EPA), 1997. Code of

Federal Regulations: Appendix B to Part 136—Definition

and Procedure for the Determination of the Method

Detection Limit—Revision 1.11. The Office of the Federal

Register, National Archives and Records Administration,

Washington, DC.

Foster Wheeler Environmental Corporation (FWEC), 1996.

Record of Decision for the On-Post Operable Unit, vol. 1,

Sections 1–11, Version 3.1.

Hermens, J.L.M., Makay, D., Mayer, P., Tolls, J., 2003.

Equilibrium sampling devices. Environ. Sci. Technol. A 37

(9), 184A–191A.

Hobbie, J.E., Daley, R.J., Jasper, S., 1977. Use of nucleopore

filters for counting bacteria by fluorescence microscopy.

Appl. Environ. Microbiol. 33 (5), 1225–1228.

Hugenholts, P., MacRae, I.C., 1990. Stimulation of aldrin and

dieldrin loss from soils treated with carbon amendments and

saturated-ring analogues. Bull. Environ. Contam. Toxicol.

45, 223–227.

Hwang, B.-H., Lee, M.-R., 2000. Solid-phase microextraction

for organochlorine pesticide residues analysis in Chinese

herbal formulations. J. Chromatogr. A 898, 245–256.

International Programme on Chemical Safety (IPCS), 1989.

Aldrin and Dieldrin Health & Safety Guide. World Health

Organization, Geneva, HSG No. 21.

Lyman, W.J., 1990. Handbook of Chemical Property Estima-

tion Methods. American Chemical Society, Washington,

DC.

Mackay, D., Shiu, W.Y., Ma, K.C., 1992. Illustrated Hand-

book of Physical–chemical Properties and Environmental

Fate for Organic Chemicals. Volume 5 Pesticide Chemicals.

Lewis Publishers, Boca Raton, p. 568.

Matsumura, F., Boush, G.M., 1967. Dieldrin: Degradation by

soil microorganisms. Science 156, 959–961.

Page, B.D., Lacroix, G., 1997. Application of solid-phase

microextraction to the headspace gas chromatographic

analysis of semi-volatile organochlorine contaminants in

aqueous matrices. J. Chromatogr. A 757, 173–182.

Ramaswami, A., Rubin, E., Bonola, S., 2003. Non-significance

of rhizosphere degradation during phytoremediation of

MTBE. Int. J. Phytorem. 5 (4), 315–332.

Zhang, Z., Pawliszyn, J., 1993. Headspace solid-phase micro-

extraction. Anal. Chem. 65, 1843–1852.