United States
                 Environmental Protection
                 Agency
 Risk Reduction
 Engineering Laboratory
 Cincinnati, OH 45268
                 Research and Development
 EPA/600/SR-92/138     Oct. 1992
EPA       Project  Summary
                  Higher  Plant Accumulation  of
                  Organic Pollutants from  Soils
                 Robert M. Bell
                   This work determines the effect of higher
                 plants on sites polluted by organic chemi-
                 cals and discusses the potential use of
                 plants as an In situ cleanup treatment
                   In situ cleanup systems have many ad-
                 vantages when compared with other
                 cleanup techniques. These systems treat
                 polluted soils, without excavating the bulk
                 of the polluted material, by detoxifying,
                 neutralizing, degrading,  Immobilizing, or
                 otherwise rendering harmless the  con-
                 taminants where they are found.
                   The first steps in developing an in situ
                 plant cleanup system for organically pol-
                 luted soils are to (1) determine the techni-
                 cal feasibility and  cost effectiveness of
                 the method, (2) determine the availability
                 of suitable plant species or varieties, (3)
                 determine whether the site possesses op-
                 timal soil conditions, (4) conduct green-
                 house scale confirmatory uptake tests, and
                 (5) confirm that the plant materials  that
                 have extracted the contaminants can be
                 disposed of in  an environmentally safe
                 manner and that the plant mass and  har-
                 vesting mechanics are realistically man-
                 ageabte.
                   This work is based primarily on litera-
                 ture review but also Includes greenhouse
                 experiments and field testwork. It is con-
                 cerned with the behavior of organic  pol-
                 lutants in the plant-soil environment, plant
                 uptake and accumulation of organic  pol-
                 lutants, and variation in uptake by different
                 plant species in different conditions.
                   The literature review involved keyword
                 searches Into suitable databases (includ-
                 ing Water Resources Abstracts, Biosis
                 Previews, Chemical and Biological  Ab-
                 stracts, Agricola, and Phytotox) and re-
                 view of over 750 scientific publications for
                 information. Within this report greater
                 emphasis has  been placed on the  few
                 reports where sufficient details concerning
                 experimental methods to make compari-
                 sons is provided.
  The greenhouse experiments Investigate
the actual extent of plant uptake of pollut-
ants from soils under known environmen-
tal  conditions. The field testwork quan-
tifies natural effects.
  The full report is not concerned  with
foodchain effects where the plant  may
accumulate pollutants, and animals feed-
ing on the plant may receive high doses
of the pollutant for subsequent effect Nor
does this report address effects of the
pollutant on the  plant  itself. As will be
seen, these effects result from interactions
between  pollutant concentrations and a
variety of environmental effects.
  This Project Summary was developed
by  EPA's Risk Reduction Engineering
Laboratory, Cincinnati,  OH, to announce
key findings of the research project that is
fully documented in a separate report of
the same title (see Project Report ordering
information at back).

Introduction
  The full report is concerned with the be-
havior of organic compounds in soils and the
potential  use of higher plants as an in situ
cleanup technique to clean up these polluted
soils. For polluted soils, in situ cleanup sys-
tems have  many advantages over other
cleanup techniques. These systems encom-
pass methods of treating polluted soils, with-
out excavating the bulk of the polluted mate-
rial,  by detoxifying,  neutralizing,  degrading,
immobilizing, or otherwise rendering harm-
less, contaminants where they are found. As
the polluted materials are not excavated, the
workforce is not exposed and pollutants do
not migrate from the site during excavation.
  The first steps in developing an in situ plant
cleanup system for organic polluted soils are
to:
  1.   determine whether vegetative extrac-
      tion from the contaminated soil has a
      high probability of being the most tech-


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      nfcaBy and cost-effective approach at
      the specific site, realizing that this ap-
      proach will require a substantial time
      period and intensive agronomic man-
      agement over that time;
  2.   determine whether suitable plant spe-
      cfes (or varieties whhin a species) are
      available to accomplish the desired
      contaminant extraction;
  3.   determine whether the site possesses,
      or can be readily modified to possess,
      soil conditions that will support optimal
      growth of the selected plant materials;
  4.   conduct  greenhouse-scale confirma-
      tory uptake tests; and
  5,   confirm that the  plant materials that
      have extracted soil contaminants can
      be adequately disposed of in an envi-
    - ronmentaliy safe manner and thaMhe
      plant mass and harvesting mechanics
      are realistically manageable.
  No limits have been placed on the meth-
ods of soH cleanup by plants, ft could  be that
the plant accumulates the pollutant for sub-
sequent disposal, or that the plant degrades
the pollutant, or that microbes attached to the
plant root degrade the pollutant
  Using  plants to ctean up organic polluted
soils, which  may prove suitable in a number
of different pollutant situations, could be most
useful for soils  contaminated by organic
chemicals to shallow depths, i.e., less than 2
meters. The maximum depth that plant roots
normally penetrate the soil is 2 meters. Such
furfaca situations are commonly encountered
from spills or leaks when the source of the
contamination is at or near the soil surface, ft
also occurs on many former dumping sites.
  Using the ability  of plants to  accumulate
pollutants and then metabolizing them to
simple units would essentially be inexpensive
to establish  and maintain, ft could, therefore,
prove extremely useful when vast volumes of
soil and sediment materials  are polluted but
not to an immediately hazardous extent These
materials may be polluted by dust bfow of by
surface erosion resulting from adjacent con-
taminated sites.
  The ability of plants to remove and accu-
mulate compounds from the soil is an essential
function  of  the  plant  Plants remove  great
amounts of applied  nitrogen and phosphorus
while they  grow and  thereby  protect the
groundwaterfrom these nutrients. Plants may
also be  able to  extract excessive levels  of
some micro-elements from polluted sites and
thereby rehabilitate the site for more normal
crops.
  The full report, based on literature review,
greenhouse experiments, and field testwork,
is concerned with:
   1.   tha behavior of  organic pollutants  in
       the plant-soil environment;
  2.   plant uptake of organic pollutants from
       the soil; and
  3.  variation in the extent of plant uptake
      by different plant species  in different
      conditions.


Literature Review

Behavior of Pollutants in the Plant-
Soil
  The study of organic chemicals in the soil
environment has been  limited to  agricultural
chemicals (e.g., insecticides, pesticides, and
herbicides) and specific compounds that cause
a problem or persist in the soil for tang periods
(e.g., PCBs,  PBBs). This has possibly oc-
curred because of the complexity of reactions,
the large number of compounds, and the cost
associated with their analysis.
 , Many_ transformations .and .processes afc_
feet an organic chemical when it is in the soil
environment. The sum of  these determine
both the compound's environmental impact
and its  life. Soil  and environmental factors
such as pH, cation exchange capacity, organic
matter,  day content, and water  content all
affect the rate and degree of these transfor-
mations. In a given situation (soil and  envi-
ronmental conditions), however, these trans-
formations  are dependent upon the physical
and chemical properties of the  compound
and therefore vary between compounds.
  The greatest influences on the  potential for
all  nontanfc organic chemicals  to affect  a
plant are the relationships and  interactions
between their  vapor,  liquid, and adsorbed
phases in the soil, and their soil degradation
rates. These processes determine not only
the form of the compound that is  available to
affect the plant but also the speed at which
the compound moves or spreads through the
soil to achieve its effect. The importance of
 each of these processes will be discussed
separately.
   The concentration of all organic compounds
 in the soil decreases with time as tang as no
further additions occur. This decrease results  -
from interactions between the compound and
 a number of physical, biological, and chemical
 parameters acting in the soil that either remove
 the compound from the soil or alter its original
 state.
   Extensive research investigated the  equi-
 librium  between the pollutant sorbed to the
 soil and that in solution in the soil water. This
 is often expressed as an adsorption isotherm,
 that, at low concentrations, approximates  a
 straight line, giving rise to the equation
         Cs = Kd{C,)
 where Cs is the adsorbed concentration (g/kg
 soil), C, is the solution concentration (g/m3 soil
 solution), and Kd (nvVkg) is the slope of the
 adsorption isotherm of the distribution coeffi-
 cient. This immediately  assumes complete
 reversibility, or an equilibrium between these
phases, that may not strictly occur for some
chemicals.
  Where the clay content of soils and sedi-
ments is relatively bw, pollutant adsorption
occurs primarily on the organic fraction of the
soil.  The degree of adsorption of the non-
ionic pollutant is then dependent on the organic
carbon content of the soil or the sediment
Variation between materials, which exhfoft a
wide range of physicochemical properties, can
then be reduced by defining an organic carbon
distribution coefficient
              '
where Kd is again the slope of the adsorption
isotherm in m3/kg, and f-,. is the organic car-
bon fraction in-the  soiTor sediment.- This
equation ultimately assumes that all organic
matter behaves in the same manner.
   Where the adsorption value of a particular
pollutant in a particular soil is not available or
has not been  measured, a good correlation
has been found between the organic carbon
distribution coefficient, K,,,., above and the n-
octanolAvater partition coefficient, K^,, of the
chemical. The K^ is defined as the ratio of
the chemical concentration in octanol to that
in water, when an aqueous solution of the
chemical is mixed with octanol and then al-
lowed to separate.
   The relationship between K^ and K^ with
different groups  of  environmentally active
chemicals and varying soil types has been
investigated with  many authors reporting
equations similar to

         tog KOO- 0.524 tagK^ + 0.62

This equation illustrates that as adsorption of
the pollutant to the soil increases, and thus
soil solution concentration of the pollutant de-
creases, log K^, increases.
   To have the greatest effect upon a plant,
the organic compourKl'rnust stay within the"
vicinity of the plant  root and not be quickly
leached away by mass flow.
   The vapor  partitioning of a compound in
the soil  is important because the speed at
which a vapor spreads through the soil in the
vapor phase is considerably greater than that
in the solution phase. Even for chemicals with
 relatively bw  vapor  densities, this transport
 route has been shown to be significant
   The relationship  between  the compart-
 mentalizatbn of the  compound between the
 soil solution and the air spaces in the soil is
often described by Henry's Law and the extent
 of partitioning is described by Henry's Con-
 stant.
   Those chemicals having a high vapor pres-
 sure, and thus a relatively high Henry's Con-
 stant, will easily move from the soil solution

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 into the soil air, will be quickly lost from the
 soil and the immediate vicinity of the plant
 root, and will have a low overall effect within
 the soil. They may subsequently be taken up
 into the plant leaf from this vapor phase; this
 is discussed later.
   There have been no all-embracing studies
 to  determine the Henry's  Constant  above
 which volatilization plays an important role in
 the transport of the compound in the environ-
 ment. It is not possible, therefore, to select a
 Constant above which transport in the soil will
 occur primarily by the vapor phase.
   The effect of the vapor phase is strongly
 influenced by the amount of water in the soil;
 limitations  in soil water mean limited partition
 from the soil water to the soil air and on the
 density or  pore space of the soil itself.
 the Transpiration Stream Concentration Fac-
 tor (TSCF) has been proposed as

 -[££•*- |jg herbicide in shoots per ml water transpired
         Hg herbicide per ml uptake solution

 In turn, it has been proposed that the uptake
 of a chemical into a plant root could be de-
 scribed by  the Root Concentration Factor
 (RCF), defined as
      RCF =
      concentration in root
concentration in external solution
 and the analogous Stem Concentration Fac-
 tor (SCF) as
      SCF =
      concentration in stem
concentration in external solution
 Plant Uptake of Organic Pollutants
   Uptake of chemicals from the soil into plants
 can be  both a complex process involving
 compound-specific or active processes and/
 or a passive process in which  the chemical
 accompanies the transpiration water through
 the  plant. When the former occurs, then a
 rigorous relationship between the degree of
 uptake and the physicochemical parameters
 of the chemical cannot be expected although
 some general trends may be evident. When
 uptake into the plant is a passive process,
 then relationships should exist.
   ft is generally accepted that a chemical in
 the soil enters a plant through four pathways:
   1.  root  uptake into the conduction chan-
       nels and subsequent transbcation by
       the transpiration stream;
   2.  uptake from vapor in the surrounding
       air;
   3.  uptake  by  external contamination  of
       shoots by soil and dust, folbwed by
       retention in the cuticle or penetration
       through it; and/or
   4.  uptake and transport in oil  cells found
       in oil-containing plants like carrots and
--- """cress."	 '   .....•-•
   The amount of a pollutant found in a plant
 growing  in organic polluted soil  will therefore
 be the sum total of each of these transport
 routes. Their respective importance depends
 on the nature of the pollutant and the soil and
 the  environmental  conditions  during  which
 plant exposure occurs.  Although the latter
 two  uptake routes may be significant in a
 local context,  they are not generally wide-
 spread and can be discounted as major routes
 of plant contamination. Because most reported
 instances of plant  uptake  of soil-borne or-
 ganic compounds make no attempt to distin-
 guish the extent of the first two uptake routes,
 the relative importance of each, under differ-
 ent environmental conditions and for different
 pollutants, cannot be assessed.
   To describe the relationship between her-
 bicide transport and water uptake into plants,
 Although the concentration factor concept is
 useful in describing the relative concentration
 in a particular plant part, ft has many limitations.
 These arise because the concentration of
 organic chemicals, both within the soil and
 within the plant, do not remain constant but
 change with time. The concentration of any
 organic chemical in  the  soil,  or in nutrient
 solution, may be depleted by plant uptake or
 degradation; the concentration of an organic
 chemical in a plant will also be reduced with
 time both by degradation within the plant and
 by the plant increasing its mass and thus
 effectively diluting the chemical.
   Research in the  early 1980s  with herbi-
 cides related both the RCF and the TSCF to
 the already defined K^ of the different groups
 of herbicides under test. TSCF shows a bell-
 shaped dependence on  K^ with  a broad
 maximum around a K^ of 1.8. The RCF in-
 creases with increasing K w and decreases
 to a  limiting value of less than unity for polar
 compounds. The explanation for this is that at
 K^ values bebw 1.8, translocatfon  is limited
 by the root concentration of the herbicide. At
-values above 1.8, transfocation is limited by
 the rate of release of the sorbed  lipophilic
 chemical from the plant root into the transpi-
 ration stream. All the TSCF in this investiga-
 tion  were, like  earlier reports, bebw unity,
 indicating that the chemicals under test moved
 passively into the shoot with the transpiration
 stream and  were  not taken  up against a
 concentratbn gradient.
   In  another experiment with more  lipophilic
 chemicals, the sorpttan of chemicals by mac-
 erated roots  was shown to be very dose to
 the RCF above, but (in contrast to the RCF)
 the sorptbn  continued to fall sharply as the
 lipophilicity decreased.  There was  a linear
 relatbnship between the concentratbn factor
 of the macerated roots and K^, shown as

 tog RCF (macerated root) = 0.77 log K^ -1.52
 This relationship  suggests that sorptbn  of
 chemical by roots is the same whether the
 root is living or dead; the sorptbn process of
 chemicals to the root is therefore likely to be a
 partitioning  event.
   In condusbn, if degradation of the chemi-
 cal does not occur within the plant and plant
 root uptake and  transbcatbn of  pollutants
 from the soil is a passive process, then plant
 uptake can be described as a series of con-
 secutive partitions between  the  soil solids
 and the soil water, the soil water and the
 plant roots, and then the plant roots and the
 transpiratbn stream, and the plant roots and
 the plant leaves.
   Pollutants with a highest fog K^ value, for
 example dfoxin  (6.14), PCBs (4.12-6.11),
 some of the phthalate esters (those with val-
 ues above  5.2), and the polycydic aromatic
 hydrocarbons (4.07-7.66),  are  those  most
 likely to  be accumulated by or in the root and
 not be translocated out of ft. Those chemicals
 with a bwer K^  (those that are lipophobb
 and water soluble) are  likely to be transfo-
 cated within the plant and may reach signifi-
 cant concentratbns within the plant leaves.
   It also seems  likely that for some of the
 more volatile herbicides at least diffusion  in
 the vapor phase and subsequent uptake by
 the  shoot may be  an  important  route of
 chemical entry into the plant. Two processes
 precede the penetratbn of chemicals in the
 soil  into leaf tissue by the air. The first pro-
 cess concerns volatilizatbn of the chemical
 from the soil.  The volatilization depends on
 the vapor pressure of the compound in the
 soil pores and it varies according to ambient
 temperatures, the water solubility of the com-
 pound,  and the  adsorption capacity and
 physical properties of the soil. The second
 process involves deposition from the air onto
 the leaf surface. As this deposition proceeds,
 the vapor pressure  of the chemical is de-
 creased and more volatilizatbn occurs.

 Variations In Pollutant Uptake by
 Different Plant Species
   A further variable affecting plant uptake of
 soil-borne organfo pollutants  is the type of
 plant being exposed to the pollutant. No sys-
 tematic examination has been made of plant
 responses to organb chemicals in soil, al-
 though  it does appear that, as with plant
 uptake of soil-borne  heavy metals,  there is
 variation in uptake both between spedes and
 within the same spedes on an individual level.
   Some of these experimental variables were
 investigated in a series of greenhouse stud-
 ies and in a field assessment.

 Greenhouse Studies
   The  greenhouse investigators  consisted
of adding pure chemical to a soil to produce a
contaminated soil. Plants were then grown in
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this soil and their accumulation of the pollut-
ant was assessed. Although environmental
conditions in a greenhouse are normally very
different from those outside the greenhouse,
the greenhouse trials produced  some very
interesting results.
   In triate with hexachbrobenzene (HCB),
the plant root concentration of the pollutant
was, in many cases, greater than that occur-
ring in the soil; this showed that pollutant
accumulation had occurred. This accumula-
tion occurred to a greater  extent with (east
oiganlc matter fraction  within the soil me-
dium, and  it  occurred increasingly with in-
creasing time. In one experiment, 33% of the
sol-tome pollutant  was accumulated from
the soB to the roots of radish within 67 days of
seed sowing. Between plant species, the abifity
to accumulate soil-borne pollutants varied.
This suggests that further work could identify
species with great affinity for cleanup.

Reid Assessment
  The field trial consisted of collecting plants
actually growing on polluted soil at a polluted
site and then comparing the root and plant
leaf concentrations with those found in the
soil surrounding the root. The results from a
dfoxin (TCDD) polluted site near St. Louis,
MO, again showed that plant roots accumu-
late soil-borne pollutants with high log K^ to
concentrations many times those found in the
soil. Plant-leaf concentrations of most  col-
lected plants were not detectable; however,
all three  replicates of one species showed
high plant-leaf concentrations of TCDD  and
this requires further investigation.
Recommendations
  This investigation  of the behavior of or-
ganic pollutants in soils and the accumulation
of these pollutants by plants has highlighted
the potential for using plants to degrade these
pollutants, either directly or through microbes
attached to the plant root. Further  investiga-
tion into these areas is merited and the prob-
ability of achieving a plant cleanup system for
polluted soils remains high.
  The full report was submitted in fulfillment
of Cooperative Agreement CR812845 by the
University of Liverpool under the sponsorship
of the U.S. Environmental Protection Agency.
  Robert M. Ball is with the Environmental Advisory Unit, Ltd., Yorkshire House,
      Liverpool L3 9AG, UK
  P. fL Sferra is the EPA Project Officer (see below).
  The complete report, entitled "Higher Plant Accumulation of Organic Pollutants
      from Soils," (Order No. PB92-209 378/AS; Cost: $26.00, subject to
      change) will be available only from:
          National Technical Information Service
          5285 Port Royal Road
          Springfield, VA 22161
          Telephone: 703-487-4650
  The EPA Project Officer can be contacted at:
          Risk Reduction Engineering Laboratory
          U.S. Environmental Protection Agency
          Cincinnati, OH 45268                                 	
 United States
 Environmental Protection Agency
 Center for Environmental Research Information
 Cincinnati, OH 45268

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