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Reviews of Environmental Contamination and Toxicology
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 Reviews of
Environmental Contamination
and Toxicology

VOLUME 210

For further volumes:

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 Reviews of
Environmental Contamination
and Toxicology

Editor
David M. Whitacre

Editorial Board
Maria Fernanda Cavieres, Valparaiso, Chile • Charles P. Gerba, Tucson, Arizona, USA
John Giesy, Saskatoon, Saskatchewan, Canada • O. Hutzinger, Bayreuth, Germany
James B. Knaak, Getzville, New York, USA
James T. Stevens, Winston-Salem, North Carolina, USA
Ronald S. Tjeerdema, Davis, California, USA • Pim de Voogt, Amsterdam, The Netherlands
George W. Ware, Tucson, Arizona, USA

Founding Editor
Francis A. Gunther

VOLUME 210

123
 Coordinating Board of Editors
D R . DAVID M. W HITACRE, Editor
Reviews of Environmental Contamination and Toxicology

5115 Bunch Road

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Archives of Environmental Contamination and Toxicology

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ISSN 0179-5953
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DOI 10.1007/978-1-4419-7615-4
Springer New York Dordrecht Heidelberg London

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Foreword

International concern in scientific, industrial, and governmental communities over

traces of xenobiotics in foods and in both abiotic and biotic environments has justi-
fied the present triumvirate of specialized publications in this field: comprehensive
reviews, rapidly published research papers and progress reports, and archival doc-
umentations. These three international publications are integrated and scheduled to
provide the coherency essential for nonduplicative and current progress in a field as
dynamic and complex as environmental contamination and toxicology. This series
is reserved exclusively for the diversified literature on “toxic” chemicals in our food,
our feeds, our homes, recreational and working surroundings, our domestic animals,
our wildlife, and ourselves. Tremendous efforts worldwide have been mobilized
to evaluate the nature, presence, magnitude, fate, and toxicology of the chemicals
loosed upon the Earth. Among the sequelae of this broad new emphasis is an unde-
niable need for an articulated set of authoritative publications, where one can find
the latest important world literature produced by these emerging areas of science
together with documentation of pertinent ancillary legislation.
Research directors and legislative or administrative advisers do not have the time
to scan the escalating number of technical publications that may contain articles
important to current responsibility. Rather, these individuals need the background
provided by detailed reviews and the assurance that the latest information is made
available to them, all with minimal literature searching. Similarly, the scientist
assigned or attracted to a new problem is required to glean all literature pertinent
to the task, to publish new developments or important new experimental details
quickly, to inform others of findings that might alter their own efforts, and eventually
to publish all his/her supporting data and conclusions for archival purposes.
In the fields of environmental contamination and toxicology, the sum of these
concerns and responsibilities is decisively addressed by the uniform, encompassing,
and timely publication format of the Springer triumvirate:

Reviews of Environmental Contamination and Toxicology [Vol. 1 through 97

(1962–1986) as Residue Reviews] for detailed review articles concerned
with any aspects of chemical contaminants, including pesticides, in the total
environment with toxicological considerations and consequences.

v
vi Foreword

Bulletin of Environmental Contamination and Toxicology (Vol. 1 in 1966) for

rapid publication of short reports of significant advances and discoveries
in the fields of air, soil, water, and food contamination and pollution as
well as methodology and other disciplines concerned with the introduction,
presence, and effects of toxicants in the total environment.
Archives of Environmental Contamination and Toxicology (Vol. 1 in 1973)
for important complete articles emphasizing and describing original exper-
imental or theoretical research work pertaining to the scientific aspects of
chemical contaminants in the environment.

Manuscripts for Reviews and the Archives are in identical formats and are peer
reviewed by scientists in the field for adequacy and value; manuscripts for the
Bulletin are also reviewed, but are published by photo-offset from camera-ready
copy to provide the latest results with minimum delay. The individual editors of
these three publications comprise the joint Coordinating Board of Editors with refer-
ral within the board of manuscripts submitted to one publication but deemed by
major emphasis or length more suitable for one of the others.

Coordinating Board of Editors

Preface

The role of Reviews is to publish detailed scientific review articles on all aspects of
environmental contamination and associated toxicological consequences. Such arti-
cles facilitate the often complex task of accessing and interpreting cogent scientific
data within the confines of one or more closely related research fields.
In the nearly 50 years since Reviews of Environmental Contamination and
Toxicology (formerly Residue Reviews) was first published, the number, scope, and
complexity of environmental pollution incidents have grown unabated. During this
entire period, the emphasis has been on publishing articles that address the presence
and toxicity of environmental contaminants. New research is published each year
on a myriad of environmental pollution issues facing people worldwide. This fact,
and the routine discovery and reporting of new environmental contamination cases,
creates an increasingly important function for Reviews.
The staggering volume of scientific literature demands remedy by which data can
be synthesized and made available to readers in an abridged form. Reviews addresses
this need and provides detailed reviews worldwide to key scientists and science or
policy administrators, whether employed by government, universities, or the private
sector.
There is a panoply of environmental issues and concerns on which many sci-
entists have focused their research in past years. The scope of this list is quite
broad, encompassing environmental events globally that affect marine and terres-
trial ecosystems; biotic and abiotic environments; impacts on plants, humans, and
wildlife; and pollutants, both chemical and radioactive; as well as the ravages of
environmental disease in virtually all environmental media (soil, water, air). New
or enhanced safety and environmental concerns have emerged in the last decade to
be added to incidents covered by the media, studied by scientists, and addressed
by governmental and private institutions. Among these are events so striking that
they are creating a paradigm shift. Two in particular are at the center of everin-
creasing media as well as scientific attention: bioterrorism and global warming.
Unfortunately, these very worrisome issues are now superimposed on the already
extensive list of ongoing environmental challenges.
The ultimate role of publishing scientific research is to enhance understand-
ing of the environment in ways that allow the public to be better informed. The
term “informed public” as used by Thomas Jefferson in the age of enlightenment

vii
viii Preface

conveyed the thought of soundness and good judgment. In the modern sense, being
“well informed” has the narrower meaning of having access to sufficient informa-
tion. Because the public still gets most of its information on science and technology
from TV news and reports, the role for scientists as interpreters and brokers of sci-
entific information to the public will grow rather than diminish. Environmentalism
is the newest global political force, resulting in the emergence of multinational con-
sortia to control pollution and the evolution of the environmental ethic. Will the new
politics of the twenty-first century involve a consortium of technologists and envi-
ronmentalists, or a progressive confrontation? These matters are of genuine concern
to governmental agencies and legislative bodies around the world.
For those who make the decisions about how our planet is managed, there is an
ongoing need for continual surveillance and intelligent controls to avoid endanger-
ing the environment, public health, and wildlife. Ensuring safety-in-use of the many
chemicals involved in our highly industrialized culture is a dynamic challenge, for
the old, established materials are continually being displaced by newly developed
molecules more acceptable to federal and state regulatory agencies, public health
officials, and environmentalists.
Reviews publishes synoptic articles designed to treat the presence, fate, and, if
possible, the safety of xenobiotics in any segment of the environment. These reviews
can be either general or specific, but properly lie in the domains of analytical chem-
istry and its methodology, biochemistry, human and animal medicine, legislation,
pharmacology, physiology, toxicology, and regulation. Certain affairs in food tech-
nology concerned specifically with pesticide and other food-additive problems may
also be appropriate.
Because manuscripts are published in the order in which they are received in
final form, it may seem that some important aspects have been neglected at times.
However, these apparent omissions are recognized, and pertinent manuscripts are
likely in preparation or planned. The field is so very large and the interests in it
are so varied that the editor and the editorial board earnestly solicit authors and
suggestions of underrepresented topics to make this international book series yet
more useful and worthwhile.
Justification for the preparation of any review for this book series is that it deals
with some aspect of the many real problems arising from the presence of foreign
chemicals in our surroundings. Thus, manuscripts may encompass case studies from
any country. Food additives, including pesticides, or their metabolites that may per-
sist into human food and animal feeds are within this scope. Additionally, chemical
contamination in any manner of air, water, soil, or plant or animal life is within these
objectives and their purview.
Manuscripts are often contributed by invitation. However, nominations for new
topics or topics in areas that are rapidly advancing are welcome. Preliminary com-
munication with the editor is recommended before volunteered review manuscripts
are submitted.

Summerfield, North Carolina David M. Whitacre

Contents

Attenuation of Chromium Toxicity by Bioremediation Technology . . . 1

Monalisa Mohanty and Hemanta Kumar Patra
The Effects of Radionuclides on Animal Behavior . . . . . . . . . . . . 35
Beatrice Gagnaire, Christelle Adam-Guillermin, Alexandre Bouron,
and Philippe Lestaevel
Illicit Drugs: Contaminants in the Environment and Utility in
Forensic Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
Christian G. Daughton
Cumulative Subject Matter Index Volumes 201–210 . . . . . . . . . . . 111

ix
Contributors

Christelle Adam-Guillermin Laboratoire de Radioécologie et d’Ecotoxicologie,

IRSN (Institut de Radioprotection et de Sûreté Nucléaire), Centre de Cadarache,
13115 Saint-Paul-Lez-Durance Cedex, France, [email protected]
Alexandre Bouron CEA, Institut de Recherche en Technologies et Sciences pour
le Vivant, Grenoble, France; CNRS, UMR 5249, Laboratoire de Chimie et
Biologie des Métaux, Grenoble, France; Université Joseph Fourier, Grenoble,
France, [email protected]
Christian G. Daughton Environmental Chemistry Branch, National Exposure
Research Laboratory, U.S. Environmental Protection Agency, Las Vegas, NV
89119, USA, [email protected]
Beatrice Gagnaire Laboratoire de Radioécologie et d’Ecotoxicologie, IRSN
(Institut de Radioprotection et de Sûreté Nucléaire), Centre de Cadarache, Bat 186,
13115 Saint-Paul-Lez-Durance Cedex, France, [email protected]
Philippe Lestaevel Laboratoire de Radiotoxicologie Expérimentale, IRSN, BP17,
92262 Fontenay-aux-Roses Cedex, France, [email protected]
Monalisa Mohanty Laboratory of Environmental Physiology, Post Graduate
Department of Botany, Utkal University, Bhubaneswar 751004, Orissa, India,
[email protected]
Hemanta Kumar Patra Laboratory of Environmental Physiology, Post Graduate
Department of Botany, Utkal University, Bhubaneswar 751004, Orissa, India,
[email protected]

xi
Attenuation of Chromium Toxicity
by Bioremediation Technology

Monalisa Mohanty and Hemanta Kumar Patra

Contents

1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2 Chemistry of Chromium . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3 Sources of Chromium in the Environment . . . . . . . . . . . . . . . . . . . . 4
3.1 Production, Sources, and Uses of Chromium . . . . . . . . . . . . . . . . 4
3.2 Chromium in Fertilizers, Animal Wastes, and Sewage Sludge . . . . . . . . . 5
4 Chromium Transport and Accumulation in Plants . . . . . . . . . . . . . . . . . 5
5 Chromium Toxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5.1 Effects of Chromium on Microorganisms . . . . . . . . . . . . . . . . . . 7
5.2 Effects of Chromium on Human Health . . . . . . . . . . . . . . . . . . . 8
5.3 Chromium Phytotoxicity . . . . . . . . . . . . . . . . . . . . . . . . . 9
6 Technology for Chromium Bioremediation . . . . . . . . . . . . . . . . . . . . 13
6.1 Microbial Remediation . . . . . . . . . . . . . . . . . . . . . . . . . . 14
6.2 Green Remediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
7 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24

1 Introduction
Human activities, such as industrial and energy production, mineral excavation, and
transportation, result in contamination by polluting substances, many of which are
dangerous. Chromium (Cr) is one of the most toxic heavy metals and is discharged
into the environment through various human activities. Extensive use of chromium
in electroplating, tanning, and textile dyeing and as a biocide in power plant cooling

M. Mohanty (B)
Laboratory of Environmental Physiology, Post Graduate Department of Botany, Utkal University,
Bhubaneswar 751004, Orissa, India
e-mail: [email protected]

D.M. Whitacre (ed.), Reviews of Environmental Contamination and Toxicology, 1

Reviews of Environmental Contamination and Toxicology 210,
DOI 10.1007/978-1-4419-7615-4_1,  C Springer Science+Business Media, LLC 2011
2 M. Mohanty and H.K. Patra

water results in the discharge of chromium-containing effluents. The pace of release

of organic pollutants, and Cr in particular, into the environment is growing exponen-
tially and is enhancing concerns that such releases pose potentially serious risks to
human health. Heavy metals, such as chromium, are not destroyed by degradation
and are therefore accumulating in the environment.
Chromium has received special attention because it is known to be toxic to
humans and animals (WHO 1988; ATSDR 2001) and to plants as well (Panda
and Patra 1997; Zayed and Terry 2003; Panda and Choudhury 2005; Shanker et al.
2005a; Nayak et al. 2008; Mohanty and Patra 2009). The World Health Organization
(WHO 1988) has addressed the toxic threats of chromium (Cr+6 ) and has listed it as
a human carcinogen (ATSDR 2001).
The Cr that contaminates soils, groundwater, and surface waters must physi-
cally be removed from many contaminated sites if these sites are to be rendered
usable. The traditional solution for dealing with Cr-polluted sites is to shift con-
taminated soil into landfills. Such a method may be effective, but is expensive and
involves exposure risks of its own. An alternative for rendering Cr-contaminated
sites suitable for sustainable development may involve use of living organisms. This
would typically include plants or microbes that are capable of degrading, absorbing,
or otherwise removing toxic materials from the environment; treatment with such
organisms would be designed to stabilize tailings (mined ore) and Cr contaminants
in situ. Such approaches are called bioremediation, and are not only feasible, but
less costly and more environmental friendly than the traditionally used approaches.
In most cases, bioremediation relies for its effectiveness on natural processes within
the selected organism. The purpose of the present review is to provide insights into
how the risks posed by chromium-contaminated sites may be attenuated at different
places worldwide, by applying the various tools and techniques of bioremediation.

2 Chemistry of Chromium
Chromium was discovered by N.L. Vauquelin in 1798. This substance is a steel-
gray, lustrous, hard, and brittle metal that belongs to Group VIB, the transition
series elements. It is the seventh most abundant element on earth and is the 21st
most abundant element in crustal rocks (Katz and Salem 1994). Cr exhibits a range
of oxidation states (Table 1). Of the many oxidation states possible for chromium,
there are two stable forms, i.e., Cr(III) and Cr(VI). The most toxic form of Cr
is Cr(VI). The primary physico-chemical properties of chromium are summarized
in Table 2. Within the normal ranges of Eh and pH in soil, chromium exists in
four states, viz., two trivalent forms (Cr+3 and CrO2− ) and two hexavalent forms
(Cr2 O7 −2 and CrO4 −2 ) (Bartlett and Kimble 1976). At a pH above 4, the solubil-
ity of chromium(III) decreases and apparent complete precipitation occurs at pH
5.5 (Bartlett and Kimble 1976). In aqueous systems, chromium exists primarily in
two oxidation states, viz., hexavalent chromium (Cr-VI) and trivalent chromium
(Cr-III) (Table 3A). Of these, Cr(III) is generally considered to be the more stable
Attenuation of Chromium Toxicity 3

Table 1 Oxidation states of various chemical species of chromium

Chemical species
of chromium Oxidation states Examples/occurrence Remarks

Elemental 0 – Does not occur naturally

Divalent Cr(II) CrBr2 , CrCl2 , CrFe2 , Unstable and oxidized to
CrSe, Cr2 Si Cr(III) stage
Trivalent Cr(III) CrB, CrB2 , CrBr3 , Occur in nature as ores
CrCl3 .6H2 O such as ferrochromite
Tetravalent Cr(IV) CrCl3 , CrF3 , CrN, Does not occur naturally
KCr(SO4 )2 .12 H2 O
Pentavalent Cr(V) CrO2 , CrF4 Does not occur naturally
Hexavalent Cr(VI) (NH4 )2 CrO4 , BaCrO4 , Rarely occur in nature,
CaCrO4 , K2 CrO4 , most toxic form,
2 Cr2 O7 produced by human
activities

Sources: Nieboer and Jusys (1988) and Katz and Salem (1994)

Table 2 Physico-chemical properties of chromium

Properties Analytical data

Phase at room temperature Solid

Color Silvery white
Atomic number 24
Atomic mass 51.996 g/mol
Electronic configuration [Ar]4s1 3d5
Electronegativity 1.66
Density 7.19 g/cm3 at 20◦ C
Hardness 9 Mohs
Melting point 1,875◦ C or 2,130.2 K
Boiling point 2,672◦ C or 2,963 K
van der Waals radius 0.127 nm
Ionic radius 0.061 nm (+3); 0.044 nm (+6)
Isotopes 6
Energy of first ionization 651.1 kJ/mol
Heat of fusion 15.3 kJ/mol
Heat of vaporization 347 kJ/mol
Heat of atomization 397 kJ/mol
Thermal conductivity 93.9 J/m s K
Electrical conductivity (1mohm/cm) 77.519
Electron affinity 64.3 kJ/mol
Atomic radius 128 pm
Common oxidation numbers +3, +6, –2, –1
Other oxidation numbers +1, +2, +4, +5
Standard potential –0.71 V (Cr3+ /Cr)

form (Banu and Ramaswamy 1997). Cr(VI) is not only more toxic than Cr(III),
the latter form of the element is also an essential trace element connected with the
glucose tolerance factor (Mertz 1969; Saner 1980). The concentration of chromium
found in various environmental media (soil, water, air, and living organisms), and
its recommended limits in such media and organisms are presented in Table 3B.
4 M. Mohanty and H.K. Patra

Table 3 Concentration of chromium found in the environment and recommended limits in

environmental media and in organisms

A Concentration limits in organisms and environmental media

Concentrations (μg/L)

Sample types Cr(VI) Cr(III) References

Fresh water life 1 8 Krishnamurthy and Wilkens
(1994), Pawlisz (1997)
Marine life 1 50 Krishnamurthy and Wilkens
(1994), Pawlisz (1997)
Irrigation water 8 5 Krishnamurthy and Wilkens
(1994), Pawlisz (1997)
Drinking water 50 50 Krishnamurthy and Wilkens
(1994), Pawlisz (1997)

B Concentrations of chromium found in various environmental media

Sample types Total ‘Cr’ concentrations References

Natural soil 5–1,000 mg/kg Adriano (1986)

30–300 mg/kg Katz and Salem (1994)
Fresh water 0–117 μg/L Pawlisz (1997)
Avg-9.7 μg/L Pawlisz (1997)
Seawater 0–0.5 μg/L Pawlisz (1997)
Air 1–5,45,000 ngm3 Pawlisz (1997)
100 ngm3 U.S. EPA (1983)
Plants 0.006–18 mg/kg Pawlisz (1997)
Animals 0.03–1.6 mg/kg Pawlisz (1997)

3 Sources of Chromium in the Environment

3.1 Production, Sources, and Uses of Chromium

The level of world production of chromium is in the order of 107 t/year. In 1998,
the production level stood at 3.4 million t. The countries that constitute the major
sources of chromite ore, from which Cr is taken, and their proportionate share
(%) are as follows: South Africa (36%), USSR (28%), Turkey (7%), India (6.5%),
Albania (6%), Finland (5%), Zimbabwe (5%), and trace amounts in other countries.
In India, approximately 98% of chromium deposits are located in the state of Orissa,
of which 94% fall in the Sukinda mining belt of Jajpur district and the rest (4%) in
the Dhenkanal, Balasore, and Keonjhar districts.
Cr is used in stainless steel alloys, which consume between 50 and 70% of total
Cr demand. Cr is also used in the chemical industry for leather tanning, pigment
production, and electroplating (Stern 1982). Chandra et al. (1997) estimated that,
in India alone, 2,000–3,200 t of elemental Cr escape into the environment annually
from tanning industry emissions. The ferrochrome industries emit 12,360 t Cr/year.
The combustion of fossil fuels, such as coal (Kessler et al. 1971) and petroleum, also
Attenuation of Chromium Toxicity 5

results in the release of chromium into the atmosphere. Coal combustion releases
520 t Cr/year. Moreover, chromium is widely distributed in rocks, fresh water, and
seawater, and these may serve as natural sources of Cr loss to the environment.
Limestone contains traces of Cr of up to 300 mg Cr/kg limestone (McGrath and
Smith 1990).
Chromium metal is used mainly for making steel and other alloys (ATSDR
1998). Cr provides additional strength, hardness, and toughness to steel. It also gives
corrosion resistance to steel. Stainless steel, high-speed steel, and corrosion and
heat-resistant steel are important varieties of chromium steel. Low-Cr steels (less
Cr and small amounts of Ni) are used in the rails of railroads, automobiles, cutlery,
and cooking utensils. Cr steel includes stainless steels (12–18% Cr) and super stain-
less steels (12–30% Cr and 7–10% Ni). The former are used to make cutlery and
cooking utensils, and the latter are used to make parts for aircraft and high-speed
trains. Chromium compounds, either in chromium(III) or chromium(VI) forms, are
also used for chrome plating, manufacture of dyes and pigments, leather and wood
preservation, and the treatment of cooling tower water. Smaller amounts are used
in drilling mud, textiles, and toner for copying machines (ATSDR 1998). Chromite
is used in refractory industry (commercial entities that use heat-resistant materials
to line the walls of high-temperature furnaces and reactors) due to its corrosion-
and high temperature-resistance and its chemically neutral character. The chromite
ore, after extraction (ore tailings), is used in the form of lumps, bricks, or cement
in linings, especially linings used in steel blast furnaces. Chromite is used to make
chromates and dichromates of Na, K, and Cr and pigments such as chromic oxide
green and chromic acid. In turn, these pigments are used in Cr-plating solutions.

3.2 Chromium in Fertilizers, Animal Wastes, and Sewage Sludge

Fertilizers and animal wastes contain chromium (McGrath and Smith 1990). The
chromium content of sewage sludge ranges from 40 to 8,000 ppm (Berrow and
Webber 1972). Fly ash from thermal plants that consume coal is often disposed of
by distributing it on land, and this constitutes another major source of Cr input to
soils. Other sources, which contribute Cr in trace amounts to the environment, are
asbestos, brake linings in vehicles, and aerosols produced from Cr catalysts used in
emission-reduction systems for treating exhaust fumes.

4 Chromium Transport and Accumulation in Plants

Chromium is similar to other heavy metals (e.g., As, Cd, Co, Cu, Ni, Sn, and Zn) in
that it is phytotoxic at a concentration above a certain threshold level (Nieboer and
Richardson 1980). Cr as a trace element is not ranked as an ‘essential element’ for
plants (Huffman and Allaway 1973). However, its essentiality for animal nutrition
has received considerable attention from those who study the role of plants as Cr
transmitters in the food chain.
6 M. Mohanty and H.K. Patra

Chromium is actively transported across biological membranes in both prokary-

otes (Dreyfuss 1964) and eukaryotes (Wiegand et al. 1985; Alexander and Ashet
1995). Once taken inside the cell, Cr(VI) is reduced to Cr(III), possibly because
of the unstable nature of chromium in intermediate states like Cr(V) and Cr(IV)
(Arslan et al. 1987; Liu et al. 1995). Evidently, Cr+3 and CrO4 −2 enter vascular
tissue with difficulty, but once they gain entry, they are readily transported to the
xylem. Hexavalent chromium in the form of CrO4 −2 moves more readily than does
Cr+3 , because the latter may be detained by ion exchange interactions on vessel
walls (Skeffington et al. 1976).
CrO4 –2 is actively transported across membranes with the help of sulfate-
containing protein carriers and, in roots, is immediately converted to Cr+3 , possibly
by an Fe(III) reductase enzyme (Zayed et al. 1998). In contrast, Cr+3 is pas-
sively absorbed and retained by cation exchange sites on cell walls (Marschner
1995). McGrath (1982) reported that despite the different properties of Cr+3 and
CrO4 –2 , there were no substantial differences in their rates of absorption and
uptake. Skeffington et al. (1976) have suggested that Cr(III) uptake does not require
metabolic energy (is a passive transport process, i.e., diffusion), whereas the uptake
of Cr(VI) ions occurs by active transport mechanisms. Translocation studies in
vegetable crops with Cr indicated that CrO4 2– is converted in roots to Cr+3 by all
plants tested (Zayed et al. 1998), and translocation of Cr from roots to shoots was
extremely limited.
Sulfate (SO4 –2 ) and other Cr(VI) anions are competitive inhibitors of chromate
and inhibit its uptake. In contrast, the presence of Ca+3 stimulates the uptake of
chromate (Shewry and Peterson 1974). Many researchers (Huffman and Allaway
1973; Lahouti and Peterson 1979; Myttenaere and Mousny 1974; Parr and Taylor
1980; McGrath 1982; Zayed et al. 1998) were of the opinion that Cr(III) and Cr(VI)
are poorly translocated to the aerial parts (shoots) of plants and tend to be largely
retained at sites in the root. Chromium is absorbed by the roots from nutrient solu-
tion as Cr+3 or CrO4 –2 . It has been found that roots accumulate 10–100 times more
Cr than do shoots (Zayed et al. 1998; Srivastava et al. 1999; Skeffington et al. 1976).
Transport and accumulation of chromium depends on the formation of complexes
that act to enhance Cr uptake and availability in plants (Athalye et al. 1995; Shanker
et al. 2005a, b; Torresdey et al. 2005; Zhuang et al. 2007). Complexes are formed
with several organic compounds, i.e., oxalic acids, malate, glycine, EDTA (ethylene
diamine tetraacetic acid), DTPA (diethylene triamine pentaacetic acid), EDDHA
(ethylene diamine di-ortho hydroxy phenylacetic acid), etc. When complexed with
different compounds, uptake rates of Cr+3 and Cr+6 varied (Athalye et al. 1995;
Shanker et al. 2005a; Zhuang et al. 2007). Metabolic inhibitors such as sodium azide
and dinitrophenol (DNP) substantially reduced uptake of Cr+6 . Alternatively, Cr+3
uptake was not affected by metabolic inhibitors in barley seedlings (Skeffington
et al. l976). In several plants (tomato, wheat, potato, bean, pea, beet, barley, maize,
spinach, etc.), Cr uptake was enhanced when supplied as Cr(III), Cr(VI), Cr-oxalate,
Cr-tartarate, Cr-EDTA, Cr-DTPA, Cr-methionine, or Cr-citrate (Cary et al. 1977a;
Athalye et al. 1995; Erenoglu et al. 2007 ). Salicylic acid complexed with chromium
substantially increased the uptake of Cr (Tripathi and Chandra 1991). This may
Attenuation of Chromium Toxicity 7

result from the fact that Cr-EDTA, Cr-DTPA, or other complexed chromium com-
pounds are not retained or impeded by ion exchange interactions with the cell walls
(Myttenaere and Mousny 1974; Athalye et al. 1995; Cary et al. 1977a).
Translocation and accumulation of chromium depends on the following major
factors: the oxidation state of chromium (Mishra et al. 1995) and the concentration
of chromium in the growth medium (Kleiman and Cogliatti 1998) or concentration
in the plant (Zayed et al. 1998). The experimental results also indicated that Cr accu-
mulation was comparatively higher in plants supplied with CrO4 −2 and Cr+6 than
in plants supplied with Cr+3 . The high concentrations of Cr in the nutrient medium
also led to an increased accumulation of Cr in plants (Zayed et al. 1998; Mishra et al.
1995). Vegetable crops, Brassica spp., sulfur-loving species (cauliflower, cabbage,
and kale), spices, and many other crops have the ability to accumulate more Cr in
roots than in other plant parts. Water hyacinth is known as a hyperaccumulator of
Cr (Lytle et al. 1998; Zhu et al. 1999).

5 Chromium Toxicity
The biological effects of Cr toxicity have been studied and reviewed by many
workers (Zayed et al. 1998; Zayed and Terry 2003; Skeffington et al. 1976;
Srivastava et al. 1999; Zhu et al. 1999; McGrath 1982; McGrath et al. 1997;
Panda and Patra 1997, 2004; Nayak et al. 2004; Erenoglu et al. 2007). Chromium
contamination is known to affect organisms in the biosphere at many locations
worldwide (Cunningham et al. 1997; Raskin and Ensley 2000; Meagher 2000).
Excess concentrations of several heavy metals, including Cr(VI), have resulted in
the disruption of both natural aquatic and terrestrial ecosystems (Gardea Torresdey
et al. 1998; Meagher 2000). The increase of Cr levels in soil and water has been
reported to cause adverse effects to microflora and growing plants. These adverse
effects are addressed below.

5.1 Effects of Chromium on Microorganisms

The toxic and mutagenic effects of chromates on microbes are also well docu-
mented. The toxic effects of Cr on bacteria and algae have been reviewed by Wong
and Trevors (1988). Mertz (1969) reported that chromium is a component of the
electron transport chain located inside the plasma membrane of prokaryotes. Cr(VI)
acts as a terminal electron acceptor as does oxygen. Ross et al. (1981) found that
10–12 mg/L of Cr(VI) was inhibitory to soil bacteria in liquid media, whereas
Cr(III) at this concentration had no effect. Ajmal et al. (1984) reported that chrome-
electroplating waste was toxic to saprophytic and nitrifying bacteria, and showed
increasing toxicity as the Cr(VI) content of the waste increased. Rhizobium has also
been observed to be very sensitive to Cr (Misra et al. 1994, 2004; Thatoi 1994;
Patnaik 1995; Mishra 2002).
8 M. Mohanty and H.K. Patra

The in vivo generation of Cr(V) from Cr(VI) by Spirogyra and Mougeotia has
been reported by Liu et al. (1995). Growth of Scenedesmus acutus was detected
at concentrations of Cr exceeding 15 ppm (Travieso et al. 1999). However, Brady
et al. (1994) reported that colonial algal growth of Scenedesmus and Selenastrum
was possible at levels of 100 ppm of Cr(III), but not at 100 ppm of Cr(VI). A
lengthening in the lag growth phase was induced by Cr(VI), whereas the growth
rate was decreased by Cr(III), in Euglena gracilis (Brochiero et al. 1984). Cr(VI)
also induced an alteration in the cytoskeleton, which may have resulted in the loss
of motility (Bassi and Donini 1984). Inhibition of photosynthesis by Cr has also
been reported in Chlorella (Wong and Trevors 1988) and in Scenedesmus (Corradi
et al. 1995). In estuarine algae, Cr(VI) toxicity is inversely proportional to salinity
(Frey et al. 1983).
In Saccharomyces cerevisiae, chromium toxicity was stronger in cells grown
in non-fermentable substrates (Henderson 1989). Other effects included inhibi-
tion of oxygen uptake (Henderson 1989) and induction of petite mutations. These
results suggest that chromate specifically targets the mitochondria of S. cerevisiae
(Henderson 1989). Additional effects of Cr in S. cerevisiae include gene conversion
(Kharab and Singh 1985; Galli et al. 1985) and induction of mutations (Kharab and
Singh 1985; Galli et al. 1985; Cheng et al. 1998).

5.2 Effects of Chromium on Human Health

Chromium pollution is known to induce respiratory and skin diseases and affect
mucous membranes (ATSDR 1998; USEPA 1998; WHO 1988). Skin ulcers that
do not heal are caused by chromium exposure. Such respiratory and skin dis-
eases were frequently found in workers at chromite mining and processing sites.
The Cr exposure also affects individuals in the nearby villages. Gastrointestinal
and neurological effects have been noted after inhalation exposure to high concen-
trations of chromium(VI). Dermal exposure to Cr(VI) also induces skin burns in
humans (ATSDR 1998; USEPA 1998; WHO 1988). Chronic inhalation exposure
to chromium(VI) in humans results in respiratory tract effects, such as perforations
and ulcerations of the septum, bronchitis, decreased pulmonary function, pneumo-
nia, asthma, nasal itching, and soreness (ATSDR 1998; USEPA 1998; WHO 1988).
Workers exposed to chromium(VI) compounds may be at risk for developing can-
cer. Based on results of animal studies, EPA has concluded that only chromium(VI)
should be classified as a human carcinogen (ATSDR 1998; USEPA 1999).
There is only limited information available on the reproductive effects of
chromium(VI) in humans exposed by the inhalation route; this information suggests
that exposure to chromium(VI) may result in complications during pregnancy and
childbirth (ATSDR 1998). Chromium(III) is an essential element in humans and has
a recommended daily intake of 50–200 μg/day for adults (ATSDR 1998). Acute oral
animal tests have shown chromium(III) to have moderate toxicity (ATSDR 1998;
USDHHS 1993).
Attenuation of Chromium Toxicity 9

5.3 Chromium Phytotoxicity

Chromium is mainly present in the environment in two stable forms i.e., Cr(III) and
Cr(VI). The activities of these two forms markedly differ because of their different
abilities to cross biological membranes (Debatto and Luciani 1988). Chromium(VI),
as chromate, readily penetrates plant cuticle and membranes via a general anion
transport system, whereas Cr(III) complexes do not diffuse through plant mem-
branes. The accumulation of chromium(III) at the cell surface results from cation
binding activity.
Several workers have reported chromium toxicity in plants (Koenig 1910; Lyon
et al. 1970; Wallace et al. 1976; Watanabe 1984; Moral et al. 1993; Misra et al. 1994,
2004). Such toxic effects of chromium includes stunted growth, chlorosis, reduced
crop yield, delayed germination, senescence and premature falling of leaves, bio-
chemical lesions, reduced enzyme activity, and reduced synthesis of proteins, amino
acids, and enzymes such as RNAse, invertase, amylase, catalase, peroxidase, and
Fe-reductase. The phytotoxic effects of chromium were first reported a century
ago by Koening (1911). Other effects from uptake of chromium by plants include
reduced rates of growth, damage to cell walls and membranes, and changes to plant
metabolic status (Williamson and Johnson 1981; Panda and Patra 1997; Nayak
et al. 2004; Mohanty et al. 2005). The visual symptoms of Cr toxicity in plants
include stunted growth, poorly developed root system, and curled and discolored
leaves (Hunter and Vergnano 1953; Misra et al. 1994, 2004). Corradi and Bianchi
(1993) also reported suppression of lateral roots as a symptom of chromium toxicity.
However, Gaw and Soong (1942) saw reduction in the dry weight and nodulation of
peas after adding chromic sulfate to the soil in which they grew. Chlorotic bands on
cereals were noted by several researchers (Kabata-Pendias and Pendias 1992; Panda
and Patra 1997, 2004; Patra et al. 2002; Nayak et al. 2004), and the exposures that
produced such effects resulted in yield reduction (Parr and Taylor 1982; Misra et al.
1994). Immediate wilting and plant death have also been reported from exposure
to very high levels of Cr (Parr and Taylor 1982). It has been reported (Austenfeld
1979; Bassi et al. 1990; Bonet et al. 1991; Choudhury and Panda 2005; Mohanty
et al. 2005, 2008, 2009; Nayak et al. 2008) that high concentrations of Cr in plants
(rice, wheat, lentil, green gram, pistia, lemna, moss, and beans) resulted in stunted
growth, reduced chlorophyll content, higher activity of certain enzymes, and higher
bioaccumulation of Cr in roots.

5.3.1 Inhibition of Germination and Seedling Growth

High levels of chromium may inhibit seed germination and subsequent seedling
growth. Cr(VI) concentrations above 2 mM can affect pea seed germination and
suppress the growth of radicle and plumule (Bishnoi et al. 1993). Chromium toxi-
city causing inhibition of seed germination and radicle growth in plants was also
observed by others (Atta Aly et al. 1999; Corradi and Bianchi 1993; Liu et al.
1993; Nayari et al. 1997; Panda et al. 2002). The germination and growth of bush
bean were substantially affected at 500 mg/kg by Cr in soil (Parr 1982). Chromium
10 M. Mohanty and H.K. Patra

toxicity that inhibits plant growth results from inhibition of cell division through
induction of chromosomal aberrations.

5.3.2 Growth Retardation

Cr(VI) is known to produce serious damage in living plant cells, but Cr(III) is
less toxic because of its extremely low solubility, which prevents leaching into
ground water or uptake by plants. At 100 μM of Cr(III), 40% growth retardation
occurs, whereas Cr(VI) showed 75% inhibition in shoots and 90% in roots of bar-
ley seedlings. At low ‘Cr’ concentrations, the dry matter content and shoot and root
length were found to increase (Bonet et al. 1991). It was also noted that marked
decreases in shoot/root ratio resulted from increasing concentrations of chromium
(Cary et al. 1997b; Zayed et al. 1998; Patra et al. 2005).
Visual and other symptoms of Cr toxicity in plants are stunted growth, poorly
developed root system, curled and discolored leaves (Pratt 1966), chlorosis and
narrow leaves (Hunter and Vergnano 1953), chlorotic bands on cereals (Kabata-
Pendias and Pendias 1992), and yield reduction (Hara et al. 1976; Hara and Sonoda
1979; Parr and Taylor 1982). Chromium has deleterious effects on plant growth
also because it causes perturbations in mineral nutrition. Cr also causes wilting and
plasmolysis in root cells (Bassi et al. 1990; McGrath 1995). After exposure to high
Cr concentrations, some plants may exhibit brownish red leaves that display small
necrotic areas, purpling of basal tissue (Adriano 1986; Hunter and Vergnano 1953),
immediate wilting, and plant death (Hara and Sonoda 1979; Parr and Taylor 1982).
Shewry and Peterson (1974) observed that the first toxic effect of Cr(VI) to
plants was inhibition of root and shoot growth. Hauschild (1993) has provided the
sequence of observed symptoms after Cr exposure in plants: induction of stress
compounds (putrescine and chitinase) > inhibition of root growth >visible damage
symptoms > leaf growth.

5.3.3 Photosynthetic Inhibition

A symptom of chromium toxicity in plants is induced disorganization of ultrastruc-
ture of chloroplast membranes (Sarkar and Jana 1987; Poschenrieder et al. 1991).
Chromium toxicity in plants leads to diminished photosynthesis (Austenfeld 1979;
Dubey and Rai 1987) accompanying reduced chlorophyll synthesis (Vazquez et al.
1987). This phenomenon results in visual symptoms in plants such as chlorosis,
necrosis, and stunted growth (Panda and Patra 2000a; Panda et al. 2003). The
inhibition of photosynthesis was due to ultrastructural changes in the chloroplast,
viz., severe decreases in granal and stromal lamellae and swelling of thyllakoid
membranes (Poschenrieder et al. 1991; Bassi et al. 1990; Choudhury and Panda
2004). Such effects are observed in several plants such as Lemna minor, Pistia spp.,
Taxithelium nepalense, and bean plants. Chromium also causes a decrease in the
Hill reaction of chloroplasts and this affects both dark and light reactions (Krupa
and Baszynski 1995; Zeid 2001).
Attenuation of Chromium Toxicity 11

5.3.4 Oxidative Stress

Chromium toxicity results in oxidative stress in plants. Such oxidative stress results
from the generation of free radicals or reactive oxygen species (ROS) such as O2 − ,
H2 O2 , • OH (Panda and Patra 2000b; Panda and Choudhury 2005). These ROS may
produce oxidative damage to biological membranes (caused by lipid peroxidation).
The basic cause of chromium toxicity emanates from the process of reduction of
Cr(VI) to lower oxidation states (Kawanishi et al. 1986), in which free radicals are
generated (Kadiiska et al. 1994; Panda et al. 2003; Choudhury and Panda 2005). The
formation of a transient form of Cr(V), during the reduction of Cr(VI) to Cr(III), is
thought to be one probable mechanism by which ROS are developed and cause their
effects in plants (Kawanishi et al. 1986). The entities responsible for the formation
of Cr(V) from Cr(VI) are physiological reducing agents such as NAD(P)H, FADH2 ,
several pentoses, and glutathione (Shi and Dalal 1989). Cr(V) complexes react with
H2 O2 to generate significant amount of • OH radicals, which may directly trigger
interactions with DNA and/or induce other toxic effects.

5.3.5 Enzymatic Changes

Several antioxidant enzymes (catalase, peroxidase, glutathione reductase, ascor-
bate peroxidase, and superoxide dismutase) may scavenge the ROS formed by the
presence of Cr. These antioxidants mitigate oxidative damage and reduce stress phe-
nomena. The activity of peroxidase and catalase has been studied in response to
chromium toxicity in several plant species: rice, wheat, green gram, and in lower
plants like mosses (Panda and Patra 1998; Panda 2003). Results show that the activ-
ities of these enzymes may be suppressed or induced. Suppressed enzyme activity
was observed in plants grown under conditions of toxic levels of Cr, but simul-
taneously, the synthesis of other enzymes was stimulated. The suppression and
induction vary with the plant species involved. Increased synthesis was observed
in catalase and peroxidase activity at 100 μM of Cr(VI), in hydroponically grown
wheat seedlings. Cr(III) may also react with the carboxyl and sulfhydral groups of
enzymes and cause alternation of their structure and activities (Bianchi and Levis
1977; Mohanty et al. 2005, 2008). Although there are several reports of the hyper-
activity of antioxidative enzymes in various plants that are under Cu, Pb, Zn stress
(Ali et al. 2003; Van Assche and Clijsters 1990), there are few reports available
on the role of enzymatic antioxidant systems in protecting plants from ROS stress
induced by Cr. This demonstrates the hypothesis of Dong et al. (2007), which is that
although antioxidants may alleviate Cr-induced stress, antioxidants may also be a
sensitive target of Cr toxicity in plants.
High concentrations of Cr cause protein degradation and inhibit nitrate reductase
activity, in some plants (Solomonson and Barber 1990; Vajpayee et al. 1999, 2000).
A decline in the content of amino acids such as cysteine (Vajpayee et al. 2001) and
increased synthesis of proline were reported to occur at toxic levels of chromium.
Moreover, a severe inhibition of cytochrome oxidase activity resulted from the bind-
ing of Cr to complex-IV and Cyt-a3 in the mitochondrial electron transport system
12 M. Mohanty and H.K. Patra

Fig. 1 The electron transport system of plants as influenced by chromium. The circled numbers
(1, 2, and 3) identify the biochemical sites of action at which chromium may generate its effects
(Panda and Choudhury 2005)

(Dixit et al. 2002). The sites in the electron transport chain that may be affected by
chromium are depicted in Fig. 1.
Fe-reductase activity was decreased in response to chromium in Fe-deficit plants
(Schmidt 1996). Chromium possesses the capacity to degrade δ-amino levulinic acid
dehydratase, which is an important enzyme for chlorophyll biosynthesis (Vajpayee
et al. 2000).

5.3.6 Macromolecular Damage

Chromium toxicity that produces damage to macromolecules has been observed in
several studies. Chromium may inhibit cell division and induce chromosomal aber-
rations (Liu et al. 1993). Cr(III) and H2 O2 cause breakage of DNA strands at a pH
of 6–8 (Strile et al. 2003). Cr also hampered the replication of DNA by inhibit-
ing transcriptional and translational processes. Binding of chromium ions to DNA
molecules is well documented to occur in mammalian (Levis et al. 1975) and ham-
ster cells (Bianchi and Levis 1977). Intracellular Cr(III) may be sequestered by DNA
phosphate groups that affect replication and transcription, and may cause mutagene-
sis (Costa 1997). Cr(III) causes modification of DNA polymerase and other enzyme
activities by displacing Mg ions.

5.3.7 Other Phytotoxic Effects

Cr(VI) depresses plant uptake of potassium and impedes H+ extrusion coupled to
K+ uptake across the plasma membrane, and may produce a decrease in the pro-
ton gradient and depolarize transmembrane electric potential energy (Zaccheo et al.
1982; Marre et al. 1974). This energy-linked process is believed to be important in
regulating certain important physiological processes such as seed germination and
stem elongation (Marre 1979). Chromium causes perturbation in the structure of the
Attenuation of Chromium Toxicity 13

Euglena cell nucleus (Fasulo et al. 1983) and in the trifoliate leaves of bush bean
(Vazquez et al. 1987).

5.3.8 Plant Response to Heavy Metals

Plants have three basic strategies for growing in metal-contaminated soil. To pro-
tect themselves from the toxic effects of heavy metals, plants may either be (a)
excluders, (b) indicators, or (c) hyperaccumulators. (a) Metal excluders act to
prevent metal from entering their aerial plant parts, or they maintain low and con-
stant metal concentrations as they grow in soils having a broad range of metal
concentrations. Such plants store absorbed metals primarily in their roots. These
plants may alter their membrane permeability, change metal-binding capacity of
cell walls, or exude more chelating substances. (b) Metal indicators are species
which actively accumulate metal in their aerial tissues at levels that generally reflect
metal levels in the soil. They tolerate the existing concentration level of metals by
producing intracellular metal-binding compounds (chelators) or alter metal com-
partmentalization patterns by storing metals in non-sensitive parts. (c) Some plant
species can concentrate metal in their aerial parts to levels that far exceed soil
levels. These are called hyperaccumulators. Such plants can absorb high levels
of contaminants and concentrate them either in their roots, shoots, and/or leaves
(Fig. 2).

Fig. 2 Conceptual response strategies of metal concentrations in plant tops in relation to increas-
ing total metal concentrations in the soil (Ghosh and Singh 2005a). Notes: Hyperaccumulators: The
plants that can absorb high levels of contaminants concentrated either in their roots, shoots, and/or
leaves. Indicators: The tolerant plant species which actively accumulate metal in their aerial tissues
and generally reflect metal availability in the soil. Excluders: The plants which prevent metal from
entering their aerial parts and restrict metal in their roots

6 Technology for Chromium Bioremediation

Heavy metals occur naturally in soils and plants and are integral components of
the biosphere. Soil contamination with heavy metals caused by human activities
is normally dealt with by transfer of contaminated soil to landfills. However, this
14 M. Mohanty and H.K. Patra

approach is expensive and causes its own problems. Therefore, eco-friendly tech-
nologies that offer low-cost alternatives are increasingly being sought to replace
the former processes. Bioremediation may constitute such an alternative for the
future. Bioremediation is the process of using living organisms, typically plants
or microbes, to remove toxic elements from the environment (Kumar et al. 1995;
Adler 1996; Cunningham and Ow 1996; Negri and Hunchman 1996; Yang et al.
1996; Kiling 1997). Usually, bioremediation takes advantage of natural processes
that already exist within selected organisms. The advantages of in situ bioremedi-
ation (bioremediation that takes place at the site of the contamination) are that it
is cheaper and it eliminates the need to extract or remove the contaminants, thus
resulting in reducing the prospect of exposure to workers. The disadvantages are
that the site of bioremediation is not contained, and it is harder to control conditions
and monitor progress.
Some bioremediation techniques are described below in greater detail. They are
broadly classified into two categories depending on the type of organisms used for
remediation.

6.1 Microbial Remediation

Many trials and studies have shown that both prokaryote and eukaryote microor-
ganisms have been successful in achieving recovery of metals from industrial waste
streams. In other studies, microbes have been utilized as biofertilizers to stimulate
the growth of plants by increasing soil fertility. It is also known that microbes may
release metal chelators or metal binders, which can help to increase absorption of
minerals from soil and reduce toxic levels of Cr. The different approaches that have
utilized microorganisms to achieve remediation are reviewed below.

6.1.1 Biostimulation
Biostimulation is the addition of nutrients, oxygen, or other electron donors and
acceptors to a site requiring mitigation of heavy metal contamination, for the pur-
pose of enhancing microbial activity of naturally occurring organisms (Leung 2004).
Biostimulation provides the basis for the requirement of retaining viable native pop-
ulations of specific contaminant-degrading microbes that already exist at the site.
Successful biostimulation may require amendment or support to achieve the correct
environment for accomplishing the degradation or detoxification of a contaminant
to an acceptable regulatory level, within a reasonable time period (Quagraine et al.
2005).

6.1.2 Bioaugmentation
Bioaugmentation is the addition of microorganisms, to those that already exist at a
site, that can biotransform or biodegrade contaminants (Quagraine et al. 2005). The
added microorganisms may be a completely new species or simply more members
Attenuation of Chromium Toxicity 15

of a species that already exist at the site. A necessary prerequisite for an efficient
bioaugmentation would be the presence of nutrients that can stimulate the growth
and activity of these “foreign” microorganisms (Quagraine et al. 2005). But the
application of this technique for removal of Cr is not currently in regular practice.
This method does not currently offer any obvious treatment advantages, in consump-
tion of time and money. Moreover, stimulating indigenous microbial populations
does not constitute, at this time, an acceptable treatment of contaminated sites. One
concept for the future is to inoculate local microbial cultures with selected foreign
microbes that have demonstrated a capability to degrade the contaminants present.
Once acclimatized to their new environment, such innoculants may be entertained
for use in bioaugmentation. However, there is the need to examine whether these
“foreign” microorganisms that are added to tailings in pond water can compete with
the indigenous populations or not (Quagraine et al. 2005).

6.1.3 Bacteria
Bacteria are generally the most commonly used organism for bioremediation.
However, fungi, algae, and plants have also been used. Bioengineering of bacte-
rial heavy metal resistance genes has produced biosensors for several toxic metals
(Ramanathan et al. 1997). Some bacteria have the ability to reduce Cr(VI) and may
be ideal for bioremediation of chromate-polluted areas (Ohtake and Silver 1994;
Wakatasuki 1995; Silver and Williams 1984; Loveley et al. 1993). Precipitation
of Cr has been reported in anaerobic Clostridium and by sulfate-reducing bacteria
(Dvorak et al. 1992).
Adsorption of Cr(III) can occur by the heat-dried biomass of the cyanobac-
terium Phormidium laminosum (Sampedro et al. 1995). Cladophora accumulated
several heavy metals, and this genus accumulated more Cr at a faster uptake rate
(72% after 15 min) than it did other metals (Vymazal 1990). Cr(III) was effec-
tively removed (83–99%) in laboratory tests with Scenedesmus, Selenastrum, and
Chlorella, whereas Cr(VI) was rather poorly removed (18–22%) (Brady et al.
1994). The removal of Cu, Ni, Al, and Cr from acidic mine wastes by the red
algae Cyanidium caldarium occurs by cell surface precipitation of metal-sulfide
microcrystals (Wood and Wang 1983).

6.1.4 Yeast and Filamentous Fungi

These organisms offer a viable alternative for the bioremediation of soils polluted
by Cr (Cervantes et al. 2001). A new siderophore, rhizoferrin, has been identified
in Mucorales that shows increased Cr(III) biosorption (Pillichshammer et al. 1995).
Chemically treated mycelia from Mucor mucedo and Rhizomucor miehei efficiently
bind Cr (Wales and Sagar 1990). The biomasses obtained from Rhizomucor arrhizu,
Candida tropicalis, and Penicillium chrysogenum were excellent biosorbents of Cr
(Volesky and Holan 1995). S. cerevisiae and Candida utilis have the ability to sorb
Cr(VI) and the sorption capacity of dehydrated cells is considerably higher than
that of intact cells (Rapoport and Muter 1995). In most cases, Cr accumulation in
16 M. Mohanty and H.K. Patra

the chromate-resistant fungi was lower than in chromate-sensitive strains, but the
biosorption and bioaccumulation processes were similar (Czako-Ver et al. 1999).
The biosorption ability of chromate-resistant mutants could be combined with their
ability to reduce chromate. Chromate-resistant strains of Aspergillus spp. (Paknikar
and Bhide 1993) and Candida spp. (Ramirez et al. 2000), isolated from Cr-polluted
environments, have shown Cr(VI) reducing activity. Moreover, there is evidence
that the heavy metal-tolerant arbuscular mycorrhizal fungi (AM fungi) could protect
plants against the harmful effects of excessive heavy metals.
In heavy metal-contaminated sites, AM fungi improve plant growth and survival
by increasing plant access to relatively immobile minerals such as P (Vivas et al.
2003; Misra et al. 2004), and this improves soil texture by binding soil particles into
stable aggregates that resist wind and water erosion (Rilling and Steinberg 2002).
Moreover, AM fungi are capable of binding heavy metals into roots in ways that
restrict their translocation into shoot tissues (Dehn and Schuepp 1989; Kaldorf et al.
1999; Misra et al. 2004). AM fungi play a vital role in metal tolerance (del Val et al.
1999) and accumulation (Jamal et al. 2002), because they store a greater volume of
metals in their mycorrhizal structures and in their roots and spores. Several heavy
metal-tolerant AM fungi have been isolated from polluted soils. These fungi can be
useful for reclamation of such degraded soils, because they are naturally associated
with many plant species in heavy metal-polluted soils (Gaur and Adholeya 2004).
Increased root/shoot Cr ratio in AM plants has also been found by Misra et al.
(2004) in chromite-mine overburden soil. The change in this ratio may point to
other mitigation mechanisms, such as dilution by increased root or shoot growth,
exclusion by precipitation into poly-phosphate granules, and compartmentalization
(Kaldorf et al. 1999; Turnau et al. 1993). Indirect mitigation mechanisms may
occur and include the effect of AM fungi on rhizosphere characteristics such as
changes in pH (Li et al. 1991), microbial communities (Olsson et al. 1998), and
root-exudation patterns (Laheurte et al. 1990). The use of dead fungal biomass of
Aspergillus niger for the detoxification of Cr(VI) from contaminated waters has
also been studied. Park et al. concluded that the mechanism of Cr(VI) removal by
dead fungal biomasses such as A. niger was a redox reaction. Cr(VI) was reduced
to Cr(III) through both direct and indirect mechanisms. The Cr(VI) removal rate
was increased with decreased solution pH and with increased Cr(VI) concentration,
biomass concentration, and temperature. Dead fungal biomass is abundant, cheap,
does not require a continuous nutrient supply for maintaining the cells in good phys-
iological conditions, and dead cells are not subjected to physiological constraints
such as metal toxicity.

6.2 Green Remediation

Phytoremediation or “green” remediation is defined as the use of green plants to
remove pollutants from the environment or to render them harmless. The generic
term ‘phytoremediation’ consists of the Greek prefix phyto (plant), attached to
the Latin root ‘remedium’ (to correct or remove an evil). This technique is a
Attenuation of Chromium Toxicity 17

cost-effective plant-based approach for removal of heavy metals from soil and
groundwater (Jena et al. 2004). The success of phytoremediation or phyto-mining
depends on the availability of plant species – ideally those native to the region of
interest – that are able to tolerate and accumulate high concentrations of heavy
metals (Baker and Whiting 2002).
There is currently considerable interest in the use of phytoremediation technol-
ogy to deal with the problem of chromium- and other heavy metal-contaminated
soils, sediments, and water. Although metal-contaminated soil can be remediated by
chemical, physical, and biological techniques, the most appropriate technique may
be determined by studying the particular category of contamination. Remediation
of metal-contaminated soil can be grouped into two categories as defined below
(Blaylock and Huang 2000; Cooper et al. 1999; Ghosh and Singh 2005a; Huang
et al. 1997).

6.2.1 Ex Situ Methods

Ex situ methods require removal of contaminated soil for treatment either on or
off site, and then returning the treated soil to the restored site. The conventional
ex situ methods that are applied to remediate polluted soils relies on excavation
and detoxification (physical or chemical destruction). Such treatments may either
destroy or may result in the contaminant being solidified or otherwise immobi-
lized. In addition, incineration of contaminants is sometimes used to effect virtual
total destruction. The conventional ex situ technique is to excavate heavy metal-
contaminated soil and then rebury it at a landfill site (McNeil and Waring 1992;
Smith 1993). Such offsite burial of contaminated media is often inappropriate
because it merely shifts the contamination problem to a new site; moreover, there
are hazards associated with the transport and redeposition of contaminated soil.

6.2.2 In Situ method

In the in situ method, remediation occurs without excavation of a contaminated site.
Reed et al. (1992) defined in situ remediation technologies as destruction or transfor-
mation of the contaminant, immobilization to reduce bioavailability, and separation
of the contaminant from the bulk soil. The use of microbial biomass and bioac-
cumulators helps to capture metals by extracellular precipitation and subsequent
intracellular accumulation; thus, the toxic metal ions are immobilized at the site
of contamination which reduces their bioavailability. In situ techniques are favored
over ex situ techniques because they are cheaper and are still effective in reducing
ecosystem impact. Diluting the heavy metal content of a substrate to a safe level
by importing it and mixing it with clean soil is sometimes an alternative for on-
site management (Musgrove 1991). On-site containment, with appropriate barriers,
provides another alternative that involves covering the soil with inert material.
Although the concept has been informally employed for at least 300 years, the
modern concept of using metal-accumulating plants to remove contaminating com-
pounds was first introduced in 1983. This technology can be applied to both organic
18 M. Mohanty and H.K. Patra

and inorganic pollutants that are present in soil (solid substrate), water (liquid
substrate), and air. The technique involves the ability of plants to absorb and con-
centrate elements of heavy metals from contaminated environmental media (soil and
water); metals that are candidates for successful uptake by plants includes Se, Hg,
Pb, Cr, Cd, Zn, and Fe. There are five categories of phytoremediation techniques:
phytoextraction using hyperaccumulator plants, phytovolatilization, rhizofiltration,
phytostabilization, and phytodetoxification (Salt et al. 1995, 1998). These processes
will be discussed in detail below.

Phytoextraction
Phytoextraction involves using plants that are capable of accumulating metals from
contaminated soils, sediments, and water, at high concentrations, into their tissues
(Peterson 1975). It is the best approach to remove and isolate soil contaminates
without destroying soil structure and fertility. It is also referred to in the literature
as phytoaccumulation (Fig. 3) (USPAR 2000). The selected plant absorbs, con-
centrates, and precipitates the toxic metals and radionuclides from contaminated
soils (Brooks et al. 1998) in their biomass. This technique is best suited for the
remediation of areas that are diffusely polluted at relatively low concentrations and
where contamination rests primarily near the surface (Rulkens et al. 1998). Several
approaches have been used, but the main two strategies for phytoextraction are

(i) Chelate-assisted phytoextraction or induced phytoextraction, in which artifi-

cial chelates are added to soil to increase the mobility and uptake of metal
contaminant.
(ii) Continuous phytoextraction, in which the removal of metal depends on the natu-
ral ability of the plant to remediate; only the number of plant growth repetitions
is controlled.

Fig. 3 Pictorial representation of the process of phytoextraction

Attenuation of Chromium Toxicity 19

Hyperaccumulator plants have been used to boost the effectiveness of this

technology. To make this technology feasible, the plants must extract large con-
centrations of heavy metals into their roots, translocate the heavy metals to surface
biomass, and produce a large quantity of plant biomass. The removed heavy metals
can be recycled through phyto-mining (Nicks and Chamber 1994; Ghosh and Singh
2005a) to produce bio-ore, which is a form of concentrated metal that is produced
from the contaminated plant biomass and may be sold (Fig. 4). Factors such as
plant growth rate, element selectivity, resistance to disease, and method of harvest-
ing are also important factors in selecting candidate plants as hyperaccumulators.
Factors like slow growth, shallow root systems, small biomass production, or dif-
ficulty in final disposal limit the use of hyperaccumulator species. Plants such as
Ipomoea carnea, Datura innoxia, Phragmites karka, Cassia tora, Lantana camara,
Brassica juncea, Brassica campestris, Leersia hexandra, Convolvulus arvensis,
Albizia amara, Cynodon dactylon, and Pluchea indica are being studied for Cr
hyperaccumulation capacity by several workers (Torresdey et al. 2004; Shanker
et al. 2005b; Ghosh and Singh 2005b; Sampanpanish et al. 2006; Zhuang et al.
2007). Some plants can accumulate remarkable levels (100- to 1,000-fold the levels
normally found in most species) of heavy metals. This striking phenomenon, known

Fig. 4 The soil, plant, and energy recovery system depicting the key components concerned with
the mass transfer and dynamics of phytoextraction (Ghosh and Singh 2005a). The soil system
involves the generation of free-metal concentration in soil from its inorganic and organic fractions.
The plant system extracts (phytoextraction) large concentrations of heavy metals into their roots,
stems, and foliage and concentrates these metals in the biomass fraction. The energy recovery
system recovers heavy metals from plant biomass for production of bio-ore and generates energy
for human needs by thermo-chemical conversion of plant biomass
20 M. Mohanty and H.K. Patra

as metal hyperaccumulation (i.e., the ability to accumulate at least 0.1% of the leaf
dry weight as a heavy metal) (Rajakaruna et al. 2006), is only exhibited by <0.2% of
angiosperms (Baker and Whiting 2002), making the selection of native species for
phytoremediation efforts a difficult task. One promising species, Typha angustifolia,
has showed high tolerance to Cr (Dong et al. 2007).

Natural Phytoextraction
In the natural setting, certain plants have been identified, which have the poten-
tial to take heavy metals up. At least 45 plant families have been identified
to have plant species that can hyperaccumulate contaminants. Some of these
families are: Brassicaceae, Fabaceae, Euphorbiaceae, Asteraceae, Lamiaceae and
Scrophulariaceae (Salt et al. 1998; Dushenkov 2003). Among the best-known
hyperaccumulator species is Thlaspi caerulescens, commonly known as alpine pen-
nycress (Kochian 1996). It is impressive that without showing injury this species
accumulated up to 26,000 mg/kg Zn and up to 22% of soil exchangeable Cd from
a contaminated site (Brown et al. 1995; Gerard et al. 2000). Brassica juncea, com-
monly called Indian mustard, has also been found to have the ability to transport
lead from its roots to the shoots.
Results of studies performed worldwide have shown that certain plants will tol-
erate high levels of metals in their tissues. For example, Ni is known to reside at
concentrations of >1,000 mg/kg in more than 320 plant species (spp.). Besides Ni,
high concentrations of other elements have also been found in many plant species
(number of species given in the parenthesis) as follows: Co (30 spp.), Cu (34 spp.),
Se (20 spp.), Pb (14 spp.), and Cd (1 sp.) (Reeves and Baker 2000). Concentrations
exceeding 10,000 mg/kg have been recorded for Zn (11 spp.) and Mn (10 spp.). The
hyperaccumulation threshold levels of these elements have been set higher because
their normal ranges in plants (20–500 mg/kg) are much higher than that for the
other heavy metals (Reeves 2003). Aquatic plants such as the floating Eichornia
crassipes (water hyacinth) (Mohanty and Patra 2007), Lemna minor (duckweed),
and Azolla pinnata (water velvet) have been investigated for use in rhizofiltration,
phytodegradation, and phytoextraction (Salt et al. 1997).

Induced Phytoextraction or Chelate-assisted Phytoextraction

Within the plant cell, heavy metal residues may trigger the production of oligopep-
tide ligands known as phytochelatins (PCs) and metallothioneins (MTs) (Ghosh
and Singh 2005a). These peptides bind and form stable complexes with the heavy
metal and thus neutralize the toxicity of the metal ions. PCs are synthesized with
glutathione as a building block and results in a peptide with the structure: Gly-(γ-
Glu-Cys-)n, {where n = 2−11}. Appearance of phytochelating ligands has been
reported in hundreds of plant species exposed to heavy metals. MTs are small gene
encoded Cys-rich polypeptides. PCs are functionally equivalent to MTs. In addition
to use of PCs, one can enhance uptake effectiveness by adding the synthetic chelate
EDTA to the soil (Huang et al. 1997). Similar results can be achieved by using
citric acid to enhance uranium uptake. The results of Huang et al. (1997) showed
Attenuation of Chromium Toxicity 21

that chelates enhance or facilitate Pb transport into the xylem, and increase lead
translocation from roots to shoots. For the chelates tested, the order of effectiveness
in increasing Pb desorption from the soil was EDTA > hydroxyethylethylene-
diaminetriacetic acid (HEDTA) > diethylenetriaminepentaacetic acid (DTPA)
> ethylenediamine di (o-hyroxyphenylacetic acid) (EDDHA) (Huang et al. 1997).

Limitations of Phytoextraction
Phytoextraction and plant-assisted bioremediation are most effective in the removal
of contaminants if soil contamination resides within 3 ft of the surface and if ground-
water is within 10 ft of the surface. It is uncertain whether an approach based on
chemical chelators is practical for improving phytoextraction, since chemical chela-
tors are also toxic to plants and may increase the uptake of metals but decrease plant
growth.

Phytovolatilization
Phytovolatilization is another type of phytoremediation. Phytovolatilization
involves the use of plants to take up contaminants from the soil, transform them
into a volatile form, and then transpire them into the atmosphere. Phytovolatilization
occurs as growing trees and other plants take up water and any associated organic
and inorganic contaminants. Some of these contaminants can pass through plant
membranes and ultimately to the leaves, where they can volatilize into the atmo-
sphere at comparatively low concentrations (Fig. 5) (Mueller et al. 1999).
Phytovolatilization has been primarily used for the removal of mercury; the
mercuric ion is transformed in plants into the less toxic elemental mercury. The dis-
advantage of this process is that mercury released into the atmosphere is likely to be
recycled by precipitation and then redeposited back into ecosystem (Henry 2000).
Bioremediation of Se and As is also possible using phytovolatilization technique.

Fig. 5 Pictorial representation of the process of phytovolatilization

22 M. Mohanty and H.K. Patra

Rhizofiltration
Rhizofiltration is a technique that can remove contaminants from flowing water and
aqueous waste streams by processing them through the extensive root system of
plants. Several aquatic plant species and hyperaccumulator plants have been used to
remove heavy metals from waste stream/water.
Rhizofiltration is defined as the use of plants, both terrestrial and aquatic, to
absorb, concentrate, and precipitate contaminants from polluted aqueous sources
that have a low contaminant concentration in their roots. Rhizofiltration can be used
to partially treat industrial discharge, agricultural runoff, or acid-mine drainage. It
can be used to remove lead, cadmium, copper, nickel, zinc, and chromium, which
are primarily retained within plant roots (Chaudhury et al. 1998; USPAR 2000). The
advantages of rhizofiltration include the fact that (a) it can be used in in situ or ex
situ applications and (b) with non-hyperaccumulator plant species. Several plants
(e.g., sunflower, Indian mustard, tobacco, rye, spinach, and corn) have been stud-
ied for their ability to remove lead from effluents by rhizofiltration. Sunflower has
the greatest ability to remove lead contamination among the tested species. Wetland
plant species such as water hyacinth (Eichornia crassipes), duckweed, smooth cord
grass, smartweed, Thlaspi caerulescens, some members of Brassicaceae family have
also been used to remove heavy metals, such as As(V), Cd(II), Cr(VI), Cu(II), Ni(II),
Se(VI), Zn, and Pb.

Phytostabilization
Phytostabilization is the process in which plants are used to transform soil metals to
less toxic forms, but without removing the metal from the soil (Fig. 6). It is mainly
used for remediation of soil, sediment, and sludges and depends on the ability of
plant roots to limit contaminant mobility and bioavailability in the soil (USPAR
2000; Mueller et al. 1999). Phytostabilization can occur through sorption, precip-
itation, complexation, or metal valence reduction (Salt et al. 1995). The primary
purpose of the plant in fulfilling its phytostabilizing role is to decrease the amount
of water that percolates through the soil matrix. This, in turn, slows or prevents the
formation of hazardous leachate and prevents soil erosion and the distribution of the
toxic metal to other areas. It is the dense root system of plants that stabilizes the soil
and prevents erosion. This approach is very effective when rapid immobilization is
needed to preserve ground and surface water, and when disposal of biomass is not
required.

Phytodetoxification
This method is an in situ process, which involves detoxification of heavy metals
through plant-based chelation, reduction, and oxidation mechanisms. Several plant
species and algae have been used in the reduction of chromium(VI) to Cr(V), and
eventually to Cr(III). Several vegetable crops and wetland plant species are also
used for remediation. Metal chelators like EDTA, DTPA, EDDHA, organic acids
Attenuation of Chromium Toxicity 23

Fig. 6 Pictorial representation of the process of phytostabilization

(carboxylic acids, salicylic acids, maleic acid), and glycine are also useful for heavy
metals remediation (Henry 2000; Salt et al. 1998).

6.2.3 Genetic Engineering to Improve Phytoremediation

To breed plants of higher biomass that have superior phytoremediation poten-
tial is an attractive avenue for improving phytoremediation. The high biomass
and productivity of a plant is genetically controlled. Therefore introduction of
such desired genes to a plant (transgenic plant) will improve the phytoremedi-
ation activity. Notwithstanding, it is crucially important to identify appropriate
plant genotypes/cultivars that are resistant/tolerant to Cr, or to other contaminants,
so that new and relevant genes become available for use in environmental reme-
diation. To achieve a better understanding of the physiological and biochemical
mechanisms of heavy metal tolerance/resistance in plants, researches in the related
areas are essential. These research areas are fundamental for discovering or cre-
ating new metal-resistant plant species. Such work has been undertaken by Dong
et al. (2007). These authors are using Typha angustifolia plant species that grow in
Cr-contaminated areas and demonstrate high resistance to Cr stress.

7 Summary
Chromium is an important toxic environmental pollutant. Chromium pollution
results largely from industrial activities, but other natural and anthropogenic
sources also contribute to the problem. Plants that are exposed to environmental
24 M. Mohanty and H.K. Patra

contamination by chromium are affected in diverse ways, including a tendency to

suffer metabolic stress. The stress imposed by Cr exposure also extends to oxida-
tive metabolic stress in plants that leads to the generation of active toxic oxygen
free radicals. Such active free radicals degrade essential biomolecules and distort
plant biological membranes. In this chapter, we describe sources of environmen-
tal chromium contamination, and provide information about the toxic impact of
chromium on plant growth and metabolism. In addition, we address different phy-
toremediation processes that are being studied for use worldwide, in contaminated
regions, to address and mitigate Cr pollution.
There has been a long history of attempts to successfully mitigate the toxic
effects of chromium-contaminated soil on plants and other organisms. One common
approach, the shifting of polluted soil to landfills, is expensive and imposes envi-
ronmental risks and health hazards of its own. Therefore, alternative eco-friendly
bioremediation approaches are much in demand for cleaning chromium-polluted
areas. To achieve its cleaning effects, bioremediation utilizes living organisms
(bacteria, algae, fungi, and plants) that are capable of absorbing and processing
chromium residues in ways which amend or eliminate it. Phytoremediation (biore-
mediation with plants) techniques are increasingly being used to reduce heavy metal
contamination and to minimize the hazards of heavy metal toxicity. To achieve this,
several processes, viz., rhizofiltration, phytoextraction, phytodetoxification, phy-
tostabilization, and phytovolatilization, have been developed and are showing utility
in practice, or promise. Sources of new native hyperaccumulator plants for use at
contaminated sites are needed and constitute a key goal of ongoing phytoremedia-
tion research programs. Such new plants are needed to enhance the attractiveness of
phytoremediation as an effective, affordable, and eco-friendly technique to achieve
successful clean-up of metal-contaminated sites worldwide.
Acknowledgments The authors are grateful to University Grants Commission, New Delhi, for
financial support under the schemes of UGC-DRS -SAP-II and RFSMS-UGC-DRS.

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offre successivement, afin de nous adoucir, des poignées de
fromage en poudre, du zamba, de la viande séchée. Nous refusons,
et il reste là, marmottant des prières. Son émotion lui donne une
étonnante activité de cuisinier, car il ne cesse de puiser dans les
sacs, d’enfoncer de la glace dans les petits pots placés devant le
feu, de mélanger la farine et le beurre dans l’eau chaude, et il nous
paraît qu’il gâte les sauces. Il mange avec ses doigts de petites
boulettes, il boit à petites gorgées cette mixture de beurre rance et
d’eau chaude.
Cela continue longtemps, sans qu’il cesse de murmurer des
« Om mané padmé houm » et de nous considérer d’un petit œil où le
moins observateur lirait une vive inquiétude.
Nous nous amusons un instant de son embarras, puis nous
engageons conversation quand tout notre monde est là. On lui
explique que si nous voulons des chevaux, c’est parce que plusieurs
de nos gens ne peuvent plus marcher et que nous ne voulons rien
prendre sans le payer généreusement. Nous l’appelons appa,
popeunn, c’est-à-dire père, frère, et il approuve en levant les pouces.
Nos chiens, qui courent sur lui avec des intentions malveillantes
lui causent un véritable effroi, et il nous supplie de les éloigner. Nous
le rassurons en lui expliquant qu’ils ne mordent pas ceux que nous
appelons « frères ». Puis nous l’apprivoisons avec du sucre, et
lorsqu’il le goûte, il ne cache pas sa joie ; puis c’est du raisin, des
abricots : il exulte, et il nous qualifie de « frères » à son tour.
Puis nous montrons des iambas et nous marchandons son
cheval. Et, pour prouver que nos intentions sont bonnes, nous
rendons la liberté à son compagnon, en lui permettant d’emporter sa
pelisse. Celui-ci est à peine à cent pas qu’il se sauve vers la
montagne, abandonnant son chef sans la moindre vergogne. Peut-
être que la consigne est de fuir.
Sur ces entrefaites arrive un cavalier ayant un fanion rouge au
canon de son fusil. Il se dit propriétaire de moutons fusillés par
Rachmed, et immédiatement nous lui offrons le thé, mais il le boit
dans sa propre tasse, qu’il tenait enfouie sous sa pelisse. Ainsi le
veulent la coutume et le rite religieux : un Tibétain ne doit pas
apposer ses lèvres à la même place que des lèvres impures. Vous
comprenez que les lèvres impures sont les lèvres des autres.
Pendant ces réflexions on a tiré du sac un lingot d’argent, on le
montre au Tibétain propriétaire, qui demande à l’éprouver. Il le frotte
sur une pierre, le regarde, y remarque un cachet, et nous lui disons
que c’est le cachet de Péking. « Pétsin ! Pétsin ! » Il est rassuré.
Néanmoins, lorsqu’on lui a pesé le prix de ses agneaux, il
examine encore l’argent ; puis, satisfait, il l’enferme dans un petit sac
pendu à son cou. Nous lui faisons cadeau d’un petit miroir : il n’en
sait pas l’usage, et d’abord ne voit pas son image reflétée. Notre
prisonnier, soumis à la même épreuve, se reconnaît et éclate d’un
rire presque idiot. Il donne avec volubilité des explications à son
congénère, lequel se regarde à nouveau et rit beaucoup en voyant
son nez et son bonnet en face de lui. Comme la nuit approche, il
nous salue et part en riant.
Notre prisonnier est parfaitement apprivoisé, et il n’hésite pas à
nous demander l’autorisation de dormir à la place où il se trouve. Il
supplie qu’on le défende de nos chiens, et exprime le désir de
posséder un petit miroir. Nous lui promettons cela pour demain.
Dès ce soir, nous lui payons son cheval, que nous attachons près
de nos tentes, où nous transportons une panoplie de fusils à mèches
et de sabres appartenant aux fuyards.
Toute la nuit nos chiens aboient, et, dans le lointain, d’autres
chiens leurs répondent. A l’heure où commence cette demi-obscurité
qui précède les jours d’hiver, des hurlements de loups éclatent dans
le silence. Ils sont, de l’autre côté du lac, toute une bande, à nous
donner le plus lugubre des concerts. Je sors de la tente à ce
moment et je trouve Rachmed déjà debout.
« Rien de nouveau ? dis-je.
— Rien ; tout va comme hier, hommes et bêtes. »
A peine suis-je rentré dans la tente qu’il arrive, et, très triste, dit :
« Imatch vient de mourir. »
 Hier encore, à l’arrivée au camp, je lui ai demandé s’il allait
mieux. « Mieux », avait-il répondu. Il avait bu du thé avec plaisir. Il
est vrai que son souffle était haletant, sa figure enflée. C’était pitié
de le voir étendre vers le feu ses doigts rouges et gonflés, qu’il
promenait sur la flamme sans les pouvoir réchauffer. Pourtant il
s’intéressait encore à ce qu’on faisait dans la tente ; je l’avais vu
poser des argols dans le foyer par habitude de vieux Kizaï, véritable
homme de steppe. Placé à l’entrée de la tente, à l’endroit qu’il
préférait, on l’avait soigneusement enroulé dans sa pelisse et ses
couvertures, et il s’était étendu pour dormir.
Lorsqu’on lui avait demandé s’il désirait quelque chose, il avait
dit : « Merci. » Nul ne croyait que sa mort fût proche. Nous
demandons à Rachmed des détails sur la dernière heure de ce
brave homme. « Quand les loups ont hurlé, Imatch a appelé :
« Parpa, aka (frère aîné), donne-moi de l’eau ; Parpa, aka, j’ai soif. »
Parpa a répondu : « L’eau est gelée, mais je vais allumer du feu, je
fondrai la glace et tu boiras. » — « C’est bien. » Puis, l’eau prête,
Imatch l’a bue sans aide, mais avec peine, et en se réjouissant
d’étancher la dernière soif. Ensuite il s’est étendu, et s’est mis à
gémir doucement. Soudain il s’est dressé, il est sorti de la tente sur
ses genoux afin de satisfaire un besoin et il est revenu à sa place.
Nous préparions le thé, on lui a offert la première tasse prête ; il a pu
la tenir. Il a essayé de boire, mais il a dû rejeter la gorgée qu’il avait
dans la bouche. Il a rendu la tasse, et se couchant il nous a
appelés : « Hé ! Timour, Iça, Abdoullah, Parpa, Rachmed. » Nous
l’avons entouré. S’étant soulevé péniblement sur son coude, il a dit,
séparant les paroles par des soupirs : « Je n’arriverai pas. Allah ne
veut pas me porter plus loin. Adieu. Je suis content de vous tous,
vous m’avez bien soigné. Adieu. Je suis mort. » Il est retombé sur le
dos, et d’un seul coup l’âme est sortie de son corps. »
Tel est le récit que nous écoutons à la lueur de notre lanterne, car
le jour n’est pas levé.
« Dès qu’il fera clair, dis-je à Rachmed, nous l’enterrerons.
Cherche un creux dans les fondrières. Il y en a d’assez grand pour y
coucher un homme. »
 Imatch nous avait suivis depuis Djarkent, depuis la frontière de
Sibérie. Tous nous l’aimions, car s’il était rude en paroles, il était
bon, courageux, travailleur. Il soignait fort bien ses chameaux, qu’il
avait autrefois possédés en partie. Étant tombé dans les griffes d’un
usurier, il avait dû lui vendre ses bêtes avec lesquelles il transportait
des marchandises, et de propriétaire qu’il était, il était devenu le
serviteur de son créancier. Celui-ci nous avait vendu les chameaux
deux fois au moins le prix qu’il les avait achetés et Imatch avait suivi
la fortune de ses bêtes. Les gages que nous lui payions étant très
élevés, il comptait faire des économies, pouvoir acheter des
chameaux à son retour, et redevenir libre, « redevenir Imatch comme
devant », ainsi qu’il disait lui-même. Mais Allah en a décidé
autrement. Le pauvre Kirghiz ne reverra plus sa steppe.
On l’étend au fond d’un trou, enveloppé du feutre qui lui servait
de lit. On lui tourne la face vers le sud-est ; il nous regardera partir et
verra la ville sainte par-dessus les océans qui embrassent le
Nouveau Monde. Les uns apportent des pierres dans le pan de leur
pelisse, les autres de la terre dans des sacs, afin de recouvrir le
mort. Puis les prières sont récitées avec des sanglots.
On fait les préparatifs de départ pour le Namtso, qui serait de
l’autre côté d’un chaînon s’allongeant en travers de notre chemin, au
dire de notre prisonnier.
Nous lui rendons la liberté, et nous lui remettons des cadeaux
ainsi que les armes prises la veille. A peine sommes-nous partis que
les fuyards d’hier apparaissent. Ils nous guettaient du haut de la
montagne, nous les voyons trotter vers leur chef.
La certitude que le Tengri Nor, que le Namtso, comme disent les
Tibétains, est là, nous donne un regain de vigueur. Nous regrettons
que nos chevaux soient incapables de nous suivre ; nous les tirons
par la bride ; ils se traînent derrière nous, car ils ne peuvent plus
nous servir qu’à porter notre selle, nos sacoches et notre manteau.
A mesure qu’on avance vers le sud, le lac semble s’élargir et
grandir aussi dans la direction du sud-ouest, et, comme la brume
nous empêche de voir sa fin, il prend l’immensité d’une mer sans
rivage. Mais la brume évanouie, on voit bien que ce n’est qu’une
petite mer, qu’un grand lac emprisonné dans les montagnes.
Le soleil du soir frappant la glace en fait jaillir des pierreries
superbes, des diamants énormes, des parures pour géants, et, entre
toutes ces merveilles d’une joaillerie féerique, éclate, isolé, un
brillant ayant les dimensions d’une colline. Nous nous souvenons
alors que nous avons devant nous le « Lac du Ciel », et cette
fantasmagorie ne nous surprend plus, un tel lac pouvant offrir tous
les spectacles. Le soleil descend, il se pose sur le sommet des
collines, et le diamant extraordinaire ne jette plus de feux : il devient
un bloc de glace, et l’écrin magique étalé devant nous semble une
eau limpide qu’aucun vent ne ride. Puis tout est rose. Le soleil
plonge derrière la chaîne ; il verse un ruissellement d’or en fusion à
l’extrémité du lac, et le paysage se silhouette en offrant ce
contraste : à notre droite, c’est-à-dire au nord, d’où nous venons, ce
sont des lignes douces, et au sud, du côté de Lhaça, ce ne sont que
lignes brisées, que crêtes menaçantes, toute une traînée de pics
semés à dessein dans le but d’élever une insurmontable barrière.
Le temps de me demander si l’on a mis le Ningling Tanla à cette
place pour nous empêcher de passer, et la nuit tombe. Les loups
poussent des hurlements lamentables.
 CHAPITRE IX
LES GENS DE LHAÇA

Après avoir dépassé le Namtso, nous sommes restés dans la

passe de Dam jusqu’au 7 mars, puis nous avons eu un premier faux
départ.
Nous avons profité de ce premier arrêt pour observer des
Tibétains de conditions diverses et des lamas venus à cette place
pour nous surveiller. Nous avions besoin de leur aide pour continuer
notre voyage et nous ne nous sommes entendus qu’après des
pourparlers qui semblaient interminables, car on est assez mal pour
bavarder à plus de cinq mille mètres d’altitude, en hiver.
Le 20 février est le premier jour de leur année, qu’ils font suivre
de cinq autres jours de réjouissances. Dès le matin, l’interprète vient
nous inviter à nous rendre chez l’amban afin de célébrer la fête.
Ce brave Mogol a coiffé une sorte de capuchon rouge pour la
circonstance et il s’est livré à des libations nombreuses, on le voit
bien. Il a les yeux plus brillants que de coutume, il répand du reste
une odeur d’arki qui nous dispense de chercher la raison de sa
bonne humeur et de la béatitude de son sourire.
« Venez, dit-il, venez vite. C’est le premier jour de la nouvelle
année. L’amban vous attend avec impatience. Il vous a préparé un
repas. Venez. »
 Nous descendons vers le camp tibétain, situé en aval du nôtre,
de l’autre côté de la glace. De nombreuses tentes noires entourent
la tente de l’amban et des principaux. C’est un va-et-vient de
serviteurs qu’aident les sauvages habitants des hauts plateaux.
Malgré la rigueur de la température, ceux-ci ont le bras droit hors de
la pelisse, et la moitié de leur corps apparaît complètement nu. Ce
sont eux qui recueillent l’argol, vont quérir la glace, dépècent les
bêtes, soignent les chevaux de selle, les mules, les yaks de bât et
enfin soufflent constamment le feu au moyen d’une outre fendue où
ils emprisonnent habilement l’air qu’ils expulsent par un tube de fer
plongé dans le tas d’argol.
Des guirlandes de prières relient les uns aux autres les sommets
des tentes, on dirait le pavoisement d’une flottille. Dans le camp il y
a un grouillement d’êtres et tout autour, sur les flancs de la
montagne, un fourmillement de yaks : ils ont servi à transporter les
provisions pour les cent ou deux cents individus qui nous honorent
de leur présence. En face de la tente de l’amban en est une autre
ouverte, servant de cuisine. Nous voyons auprès, un homme faisant
les gestes de battre le beurre dans une jarre : c’est, paraît-il, afin de
mélanger le beurre au thé : les Tibétains boivent ce mélange avec
plaisir.
L’amban, leur chef laïque, nous attend devant sa tente, il envoie
quelques serviteurs assurer notre marche sur la glace en nous
tenant par le bras, car nous sommes des hôtes précieux. Nous
grimpons la berge au bas de laquelle on doit marcher avec
précaution, et l’amban s’avance au-devant de nous. Une fois de
plus, nous constatons qu’il n’est pas grand. Il nous accueille avec un
sourire traversant sa lune ronde et glabre ; son front découvert de
vieille fille qui perd les cheveux vers la quarantaine nous semble
marquer beaucoup d’intelligence. Il nous fait entrer les premiers
dans sa tente de toile à quatre faces, formée par des portants sur
lesquels se pose un toit pointu également à quatre faces. Comme
l’amban est un laïque, il n’emploie que des laïques pas tondus, et un
serviteur à cheveux longs, à tresse pendante, soulève la portière.
 L’amban nous invite à nous installer sur une sorte d’estrade, à
droite de la porte. Une autre estrade un peu plus haute, adossée au
fond de la tente, lui est réservée. Il s’y assied, jambes croisées, sur
une peau de tigre, s’adossant à des coussins, doublés les uns de
soie de Chine, les autres de calicot des Indes, si je ne me trompe.
Puis, sans plus tarder, nous lui demandons à quelle date viendra
la réponse de ses supérieurs, permettant l’organisation de notre
départ.
« Vite, dit-il.
— Vous seriez bien aimable de nous dire ce que vous entendez
par le mot « vite », car dans certains pays cela veut dire : « Au bout
d’une heure vous aurez ce que vous demandez » ; dans d’autres :
« Après un jour ou une année ». Et chez vous quel sens à Ce
mot ? »
Le traducteur mogol nous paraît plus que jamais sous l’influence
de l’arki et il commence par rire de bon cœur, puis il traduit ces
paroles, et l’amban rit à son tour.
« Il est vrai, dit-il, que l’on doit s’entendre sur le sens des mots.
Je puis vous dire que « vite » signifie dans six jours environ, car nos
chefs auront sans doute besoin de consulter le mandarin chinois. Or
il est absent de Lhaça et il habite à l’ouest, à deux journées de la
ville. Croyez que je regrette ces retards, mais ils sont inévitables. »
Sur ces entrefaites, entre le chef des lamas ici présents, et il
s’assied à gauche de l’amban. Devant eux, une petite table supporte
leurs tasses que surmonte un couvercle en argent. Des jeunes gens
versent fréquemment du thé au beurre contenu dans des théières en
terre cuite.
Tous se disputent l’honneur de nous servir afin de nous
examiner. L’un d’eux a sans doute pris la théière des mains d’un
camarade qui veut l’empêcher de pénétrer dans la tente et le retient
par le pan de sa robe. Pour se dégager, il lance derrière lui de
vigoureux coups de pied tandis qu’il soulève la portière avec le plus
aimable des sourires.
 A gauche de l’amban, un autel a été installé sur des coffres :
l’image de Bouddha enfermée dans un cadre doré sourit ; devant
sont alignées sept petites coupes en cuivre contenant du safran et
de l’huile ; un luminaire flambe doucement ; des aromates brûlent
dans une cassolette ; des bâtons d’odeur se carbonisent lentement,
plantés dans les cols de petites théières. On a déposé sur les deux
degrés de l’autel des figurines en beurre ; je puis distinguer une tête
de mouton à cornes ayant sur le front des protubérances en sucre
blanc, des colonnettes en même matière, et, dans des soucoupes,
des confiseries offertes en holocauste à la divinité.
Après avoir bu un nombre considérable de tasses de thé, nous
manifestons le désir de nous retirer. L’amban, appuyé par son chef
des lamas, nous réitère ce qu’il a dit vingt fois déjà.
« Tâchons d’arranger les affaires, d’être toujours d’accord, d’être
toujours comme cela », et ce disant, il joint les index par la face
interne, et, insistant pour que nous soyons amis, il se sert de cette
comparaison :
« Deux tasses d’une belle porcelaine posées sur une table font
un bel effet. On les entrechoque, elles se cassent, et il n’y a que
débris. Ne nous entrechoquons pas, ne nous entrechoquons pas »,
répète-t-il en se levant pour nous reconduire.
A la sortie, tout le monde nous salue en souriant et l’on voit bien
que la consigne est de ne pas nous choquer.
Sous prétexte de nous promener, nous nous dirigeons vers une
tente noire qu’on a dressée depuis peu sur le chemin de la passe en
amont de notre camp. Nous voyons accroupis autour d’un feu
d’argol huit hommes à longue chevelure qu’un lama tondu
commande. Ils se tiennent au fond d’un trou, ils bavardent
tranquillement, fumant une petite pipe à fourneau de terre et à tube
en os qu’ils se passent à tour de rôle. Ce sont de pauvres diables
chargés de ramasser l’argol et qui ne célèbrent pas du tout la fête de
la nouvelle année. Ce que nous prenions pour une tente, de loin,
n’est qu’une moitié de tente, un abri de bure noire ouvert du côté où
le vent ne souffle pas. Les Tibétains y dorment sur un peu de menue
paille mêlée à des argols ; dans un coin sont entassés leurs arcs et
leurs lances, et au milieu trois pierres forment le foyer pour les jours
où le vent souffle fort. Leur costume rudimentaire est taillé dans des
peaux de mouton effiloquées dans le bas, trouées et d’une saleté
extraordinaire. Leurs figures, noires de graisse et de fumée,
contribuent à réaliser le type le plus pur du sauvage qu’on puisse
imaginer.
En considérant ces crânes étroits, on se demande quelles
cervelles ils peuvent bien abriter, et nous ne nous étonnons pas que
les lamas exercent un ascendant extraordinaire sur des êtres aussi
peu intelligents, aussi peu susceptibles de volonté, dont les
sensations doivent être à peu près celles de leurs yaks et de leurs
chiens. Espérons que tous les Tibétains ne ressemblent pas à cette
bande de bêtes à face humaine.
Le 21 février, par un vent d’ouest, les fêtes continuent : on sonne
les trompes en haut des rochers, on chante dans le camp, et les
guirlandes de prières sont agitées par le vent.
Le 1er mars, dès le matin, le ciel est couvert, puis un ouragan se
déchaîne et la vallée disparaît sous la poussière. Le vent souffle
toute la nuit, quelques tentes des Tibétains sont emportées par la
bourrasque et nous nous trouvons très bien dans la nôtre, qui est
quadruple : en effet, l’amban nous a fait cadeau d’une tente double,
que nous avons jetée sur la nôtre, et cela nous permet d’avoir un
réduit à l’arrière pour divers objets, et un vestibule à l’entrée. De
grosses pierres consolident notre habitation, et notre toile défie le
vent. Le minimum de la nuit est de − 23°,5, aussi, au réveil, notre
troupe se plaint du mal de tête. Les ouragans amènent toujours une
recrudescence du mal de montagne, même pendant les repos.
Ce 2 mars, vers midi, un nuage de neige passe sur nous ; le ciel
reste couvert avec un vent de nord-ouest qui n’est que le vent
d’ouest du Namtso s’engouffrant dans le col.
Dans l’après-midi, l’interprète à la dent longue nous apporte un
peu de lait, que nous réclamons depuis longtemps pour nos
malades, et en même temps il nous fait part de la prochaine arrivée
de grands chefs. Nous nous en étions doutés dès le matin, car de
nombreux yaks chargés étaient arrivés dans la nuit et nous avions
vu dresser une grande tente avec beaucoup de difficultés, et même
nous avions ri lorsqu’un coup de vent avait enlevé la toile. Le remue-
ménage, le va-et-vient des hommes, les petits chefs surveillant les
travaux, nous avaient mis en éveil, et l’indiscrétion de l’interprète ne
servait qu’à préciser nos prévisions.
Aussi, cet homme parti, nous nous postons à une bonne place
avec nos lorgnettes et nous surveillons la descente de la passe.
D’abord arrivent des chevaux chargés, bien harnachés, ayant au
cou des sonnettes sonores ou des houppes de couleur rouge,
couleur du pouvoir. Puis, voici des cavaliers bien vêtus ; ils errent à
travers les fondrières et paraissent ignorer le sentier tracé au bas
des contreforts et qu’on atteint avec un détour. Des sauvages à
longue tresse les appellent ; d’autres s’empressent à leur rencontre,
prennent les brides et soutiennent leurs montures sur la glace. Ils
arrivent au camp et toutes les tentes se vident, on se presse autour
d’eux. Ce n’est que l’avant-garde, car l’agitation reprend dans le
camp tibétain et des serviteurs se dirigent vers la passe.
Bientôt apparaissent les grands chefs, montés sur des chevaux
au pas rapide et sûr, entraînant les hommes qui les tiennent par la
bride sous prétexte de les soutenir, et peut-être par politesse. Nous
distinguons trois grands personnages. Couverts de fourrures
doublées de soie jaune, ils paraissent ventrus, rebondis, énormes, et
l’on s’étonne qu’ils n’écrasent pas de cette masse leurs agiles petits
chevaux. Sur la tête, ils ont les chapeaux à plume des mandarins
chinois, mais posés sur une cagoule qui leur garantit la nuque et la
face, dont on ne voit rien ; leurs yeux sont en outre abrités par des
lunettes protubérantes que surplombe une visière par surcroît de
précaution. Une escorte assez nombreuse, aux costumes bigarrés,
trottine derrière eux avec un grand bruit de grelots. Ce spectacle
offre une certaine pompe, mais il nous semble ridicule et nous
pensons à un défilé de mi-carême.
Dans le camp tous les chefs civils et religieux attendent placés
sur une ligne les mandarins ; là ils s’inclinent profondément en
restant à leur place. Seul l’amban s’approche, complimente deux
des arrivants, avec lesquels il échange une poignée de main ; ceux-
ci, sans descendre de cheval, gagnent les tentes qui leur sont
destinées. La foule se disperse et chacun court où sa besogne
l’appelle.
Lorsque nous réfléchissons que tout ce rassemblement de
peuple a lieu parce que nous sommes ici, nous trouvons qu’on nous
fait beaucoup d’honneur.
Puis, les interprètes viennent nous demander si nous voulons
accorder une audience aux grands personnages qui sont arrivés.
Nous disons que nous serons trop heureux de les recevoir
immédiatement. Notre réponse transmise, toute une troupe se dirige
vers nous, ayant en tête deux individus somptueusement vêtus à la
chinoise. Ils avancent bras dessus bras dessous, et l’un d’eux, petit,
court, rond, voûté, s’appuie sur son compagnon. Ces deux
vénérables marchent lentement, reprennent haleine tous les quinze
pas. Nous restons impoliment sous notre tente et nous n’en sortons
que quand la troupe est sur notre territoire.
Nous échangeons des saluts avec ceux qu’on nous présente
comme le ta-lama et le ta-amban. Des porteurs déposent à nos
pieds, ou plutôt sur notre provision d’argols, cinq sacs : un sac de
riz, un de zamba, un de farine, un de pois chiches, un de beurre. Là-
dessus nous invitons les deux ambassadeurs à s’abriter sous notre
tente, où des feutres les attendent. La simplicité de notre
ameublement les effarouche sans doute un peu, car ils ont l’air
d’hésiter, ils font des difficultés avant d’entrer. Ils demandent la
permission de s’asseoir sur leurs petits tapis, et leurs serviteurs
étendent pour l’un une peau de guépard, pour l’autre un petit
matelas doublé de soie. Ils excusent ces précautions en disant :
« Nous sommes vieux et fatigués. »
Les trois premiers négociateurs s’assoient auprès d’eux, en face
de nous, et la conversation commence. D’abord ce sont des
politesses :
« Comment vous portez-vous ? dit le ta-lama.
 — Fort mal, car nous sommes dans une mauvaise place. »
Cette réponse ne laisse pas de les désorienter un peu, ils
s’attendaient à plus d’amabilité de notre part, et notre connaissance
le petit amban baisse la tête. Il nous avait dépeints comme des gens
convenables, et, pas du tout, nous répondons avec rudesse.
Nous leur demandons à notre tour s’ils ont fait un bon voyage.
« Oui, quoique la route soit mauvaise. Nous avons dû venir à
petites étapes, à cause de notre âge. Les fêtes nous ont aussi
retardés, sans quoi vous nous auriez vus plus tôt. Ces fêtes sont
commandées par la religion, et nous devons les célébrer. »
Ensuite viennent des questions sur nos personnes, sur le but de
notre voyage, et nous répondons ce que nous avons déjà dit vingt
fois au petit amban. Et ils nous font les mêmes propositions que ce
dernier nous a déjà faites :
« Vous allez retourner sur vos pas !
— Non. Cela est impossible.
— Retournez, nous vous procurerons tout ce qu’il vous faudra.
C’est ce que vous avez de mieux à faire. Nous nous quitterons bons
amis. Réfléchissez à ma proposition, et je vous le conseille,
acceptez-la : j’espère que nous nous arrangerons à l’amiable, car
nous sommes venus sans soldats, et nous aurions pu en amener de
Lhaça. Cela vous prouve nos bonnes intentions.
— Il est inutile de nous proposer le retour et de nous conseiller
de réfléchir. Nous ne parlons pas à la légère. Nous sommes venus
de l’Occident, poussés par un destin, par une force qui nous a
transportés à travers les déserts en suivant un chemin que vous-
mêmes ignorez. Notre volonté est d’aller à Batang et de rejoindre
nos compatriotes au Tonkin, où ils habitent sur les terres prises à
l’empereur de Chine. Vous ne pouvez rien contre notre volonté, nous
ne ferons pas un seul pas vers le nord, soyez-en persuadés. Vous
ne nous effrayez pas, nous venons de l’extrémité de la terre sans
avoir pu être arrêtés, nous poursuivrons notre marche et vous nous
y aiderez. Vous réfléchirez vous-mêmes et vous verrez que Bouddha
lui-même en a décidé ainsi. Nous préférons mourir plutôt que de
retourner. C’est notre dernier mot. »
Le soleil se couchant, ils se lèvent et s’éloignent, visiblement
mécontents d’avoir entendu de semblables paroles en présence de
leur escorte.
Ils nous disent adieu, et, avant de s’éloigner, voulant avoir le
dernier mot, le ta-lama nous répète :
« Réfléchissez. Réfléchissez. »
A quoi je réponds en français, irrespectueusement :
« Oui, mon vieux.
— Que dit-il ?
— Il vous souhaite bonne nuit dans sa langue », répond
Abdoullah.
Les deux grands chefs s’éloignent et nous restons aux prises
avec le petit amban et les deux autres négociateurs des premiers
jours.
Le petit amban — qui nous a pris en affection, nous
commençons à le croire — nous fait des reproches :
« Pourquoi avez-vous parlé sur ce ton à mes chefs ? Songez
donc que ce sont les deux premiers de Lhaça, ils peuvent autant que
les kaloun (ministres). Soyez plus aimables demain. Dites-moi ce
que vous désirez. Je leur parlerai dans ce sens. Mais ne changez
pas d’idées, car si vous me contredites ensuite, ils m’accuseront de
m’être vendu à vous et d’avoir pris en main vos intérêts et même
cherché à obtenir pour vous plus que vous ne vouliez.
— Notre désir est d’aller à Batang, ainsi que nous vous l’avons
cent fois répété. Vous nous fournirez les moyens de transport, des
vivres, et nous vous les payerons. C’est ce que nous voulons
aujourd’hui et ce que nous voudrons jusqu’à ce que nous
l’obtenions.
— Je le dirai à mes chefs, mais sans pouvoir insister, car ils se
défieraient de nous, ils nous accuseraient et nous serions punis
terriblement. »
 Il s’éloigne sur ces mots. Nous allons nous asseoir près de notre
feu d’argol et nous échangeons nos impressions sur les deux
ambassadeurs.
On reste longtemps à bavarder au clair de la lune. On entend
Abdoullah réciter des prières en compagnie du Doungane, sous la
tente duquel il est allé se réfugier. C’est le signe qu’ils ne voient pas
l’avenir en beau, car ils s’adressent toujours au ciel dans les
mauvais moments. Les temps sont-ils meilleurs ? ni Abdoullah ni le
Doungane ne récitent une fatiha.

. . . . . . . . . . . . . . . . . . . .

Les pourparlers avec les deux grands chefs continuent le 3 mars

et les jours suivants, et après des phases diverses, des fâcheries et
des raccommodements, nous arrivons à les convaincre que nous ne
sommes ni Anglais, ni Russes, mais Français. Et nous obtenons un
déplacement pour le 7 mars.
« Enfin, nous allons lever le camp, disons-nous, et changer de
place. »
Le matin du 7 mars, le soleil luit, il a neigé les jours précédents et
la montagne est resplendissante, éblouissante. C’est un superbe
temps de départ, mais un faux départ, car nous nous déplaçons pour
nous installer dans une meilleure place, où nous attendrons encore.
Le camp est très animé. Il ne faut pas moins de trois ou quatre
cents yaks ou chevaux pour transporter les bagages, les tentes et
les vivres. De tous côtés on voit les hommes noirs courir derrière
leurs bêtes, les rassembler, les pousser devant eux avec des
sifflements aigus et en faisant tournoyer leurs frondes. Pour n’être
point gênés dans leurs mouvements, ils ont tiré leurs bras hors des
manches de leurs pelisses, qui leur tombent sur les reins et laissent
leurs torses à nu. Leurs longues tresses les embarrassent lorsqu’ils
se baissent et ils en ceignent leur front. Ils paraissent avoir des
bandelettes comme de chastes matrones romaines, ou bien des
diadèmes, et l’on dirait ces barbares que, dans les jeux publics, on
déguisait en rois pour l’amusement de la populace.
Ces Tibétains aussi sauvages que leurs bêtes ont grand’peine à
les saisir. Nos chameaux les épouvantent. Et ce n’est pas du
premier coup que les yaks se laissent prendre par la corne d’où l’on
détache le cordon attaché à la cheville qui perce leur mufle. Leurs
maîtres les approchent avec précaution et ne les saisissent que par
surprise. C’est bien pis pour les charger : il faut un temps infini avant
de pouvoir ficeler sur leur dos nos coffres, dont ils ne veulent à
aucun prix. Mais la patience de ces hommes est sans borne, et ils
finissent toujours par avoir raison de l’animal récalcitrant ; dès qu’ils
le tiennent, ils l’entravent, le chargent malgré les ruades et les coups
de cornes, mais ne le châtient pas.
Des lamas, le bâton à la main, leur donnent des ordres, les
réprimandent. Ces sauvages exécutent gaiement leur besogne : ils
sont très obéissants, très respectueux à l’égard de leurs lamas : ils
leur parlent et ils les écoutent dans la plus humble posture, courbés
en deux, la langue pendante.
Tous nos chevaux étant morts, on a sellé pour nous, de petits
chevaux tibétains pleins de feu. Ils sont mangeurs de viande crue,
ainsi que nous nous en sommes assurés de nos propres yeux. Ces
carnivores ont des jambes merveilleuses, une adresse acrobatique,
ils se tiennent en équilibre sur la glace, sur les mottes des tourbières
limoneuses, et, s’enlevant, bondissant sur le sentier, ils nous
emportent avec un trottinement rapide auquel nous ne sommes plus
habitués. On dirait que les petits diables nous trouvent légers
comme des plumes ; au fait, notre embonpoint est nul, notre
maigreur est ascétique.
En trois heures et demie nous chevauchons 22 verstes par
monts et par vaux, mais surtout en descendant. Nous allons camper
près d’une rivière gelée qui verse ses eaux au Namtso.
Le petit amban nous reçoit sous sa tente, où il nous a préparé un
repas délicieux. C’est d’abord une langue de yak fumée, à laquelle
succède une autre langue de yak, que nous faisons disparaître, y
compris les environs de l’œsophage ; puis des légumes, des
carottes salées de conserve, et du poivre rouge et vert ; enfin des
galettes de pain sans levain, et du thé au beurre à discrétion. Cet
excellent amban admire notre appétit et nous excite à le satisfaire.
Avouons que nous n’avons pas besoin d’encouragement.
L’amban nous a reconduits près de notre camp, posé sur la rive
droite du cours d’eau. Il voulait nous retenir sous sa tente jusqu’à ce
que la nôtre fût dressée, mais nous avons manifesté le désir de
marcher, parce que nous avons froid aux pieds, et il nous a
accompagnés disant :
« La coutume ne veut pas qu’on laisse seul un hôte sans abri. On
doit lui tenir compagnie. »
Nous profitons de cette coutume pour lui poser diverses
questions. D’abord c’est le nom de la belle chaîne que dominent les
pics Huc et Gabet. Ils ont ce soir chacun un turban de nuages, cela
me rappelle la Perse et le turban bien connu du Demavend. Cette
chaîne s’appellerait Samda Kansain, et la rivière au bord de laquelle
nous nous trouvons, Samda Tchou, empruntant son nom à la
montagne qui la nourrit.
Ensuite nous lui parlons du serou, de la licorne dont le père Huc
a entendu certifier l’existence. Après des explications, nous
apprenons que cet animal vit au pays du Gourkas (dans l’Inde) et
qu’il a une corne non pas sur le sommet de la tête, mais sur le nez,
et que c’est du rhinocéros qu’il s’agit.
8 mars. — Le vent souffle d’ouest. Il neige par instants. Le soleil
paraît, disparaît. Puis, la violence du vent plus grande, le ciel se
couvre et le froid est insupportable après la tiédeur de l’après-midi.
L’amban vient nous entretenir. Il nous engage à prendre
patience. Car il faut qu’on nous prépare à Lhaça les objets que nous
avons demandés. Avant de quitter Dam, on a dressé, sous notre
dictée, une longue liste de nos désirs.
Nous avons demandé des costumes de tous genres, des
chaussures, des coiffures, les objets de culte, les cymbales grandes
et petites, des peaux, des prières même. On nous a promis de réunir
des chevaux pour nous, et de les expédier vite ici. Mais l’amban
craint notre impatience. Il se rend compte de l’envie que nos gens
ont de partir. Personne d’entre nous ne se soucie de rester ici, à
commencer par moi. Cependant il y a des degrés dans l’impatience,
et jusqu’à nouvel ordre nous avons le devoir d’attendre, car les
Tibétains ne nous témoignent aucune malveillance.
L’amban proteste de la pureté de ses intentions. « Vous êtes des
frères pour nous. Nous voulons vous être agréables. Si nous vous
retenons, c’est parce que mes deux supérieurs doivent écrire à
Lhaça. Ils sont convaincus que vous êtes des gens de bien. Mais,
que voulez-vous, nous n’avons pas vos habitudes, nous ne savons
pas expédier vite les affaires. Un conseil décide des affaires
importantes, et vous savez que les membres d’un conseil nombreux
ne tombent pas immédiatement d’accord. Si j’étais seul, vous auriez
de suite ce qu’il vous faut, mais rien qu’ici nous sommes trois grands
chefs et vingt petits environ. Les uns se défient des autres et il faut
beaucoup de prudence pour ne pas être accusé. »
Cette crainte d’être accusé que l’amban a manifestée déjà
semblerait prouver que Lhaça est un foyer d’intrigues, que le pouvoir
y est partagé, qu’il est très recherché, et que ceux qui le possèdent
se montrent jaloux de le conserver.
L’amban demande des renseignements sur la façon dont on vit
en France ; quelle situation est faite aux femmes ; sont-elles jolies ?
Puis il parle des inventions étonnantes que les Anglais ont
appliquées dans les Indes et qu’il n’a pas vues. « Avez-vous aussi
des machines ? Avez-vous aussi de grands bateaux avançant sur
l’eau sans voiles ? Et des livres ? »
Et apprenant que nous possédons beaucoup de livres traitant de
toutes les questions auxquelles l’homme s’intéresse, il s’étonne que
nous voyagions.
« Car, dit-il, à quoi bon parcourir les pays lointains lorsqu’on peut
occuper sa vie à lire sans quitter son foyer. Ainsi je n’ai moi-même
aucun désir de sortir du Tibet : les livres de notre religion suffisent à
ma curiosité. »
 L’amban n’a évidemment pas d’idées modernes, son esprit n’a
pas besoin de l’activité fébrile où nous nous complaisons, il est
heureux de vivre sans efforts dans son pays, il ne se soucie pas des
« grands problèmes » de l’humanité, le progrès n’existe pas pour lui ;
il fait de la politique autant que l’exige l’instinct de conservation, il lit
et relit un livre, marmotte des formules incompréhensibles et il est
heureux. Ses actions n’ont qu’un but : conserver le fromage où sa
naissance l’a placé, et peut-être, si cela est possible sans trop de
risque, évincer son supérieur du fromage de Hollande plus gros que
le sien, et s’y fourrer avec la satisfaction du devoir accompli. C’est
surtout en ceci que l’amban ressemble aux gens d’Europe. Du reste,
c’est un homme très aimable. Il a peut-être raison de ne pas
s’intéresser au reste du monde.
 CHAPITRE X
LES GENS DE LHAÇA

(SUITE.)

Le 14 mars, on nous invite à déjeuner chez le ta-lama, en

compagnie du ta-amban et de l’amban. Un repas de gala a été
préparé à notre intention ; il dure quatre heures, pendant lesquelles
nous pêchons avec nos bâtonnets dans une trentaine de plats
rarissimes et qui doivent coûter excessivement cher. En effet, il n’est
pas facile de se procurer au Tibet des jeunes pousses de palmier,
des dattes de l’Indoustan, des pêches de Lada (Leh), des jujubes de
Ba (tang), des petites baies de Landjou, des algues de mer, des
mollusques des bords de l’océan, etc.
Malgré cette profusion, le ta-lama regrette de ne pouvoir faire
mieux les choses, attendu qu’il est loin de la ville et que les
transports sont difficiles. Il espère que nous l’excuserons, car c’est
un repas d’amis. Toutefois, parmi ces divers produits de l’art
culinaire asiatique, quelques-uns sont mangeables et nous leur
marquons toute notre considération. Mais le lait chaud, qu’on nous
sert en quantité suffisante, est ce que nous préférons à tout, nous
nous plaisons à y plonger des dattes de l’Indoustan pour les dégeler.
L’abondance et l’excellence du repas n’amollissent pas nos
cœurs, et nous ne nous laissons pas fléchir lorsque, les petites
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