The Science of the Total Environment 213 Ž1998. 57]64
Use of epiphyte plants as biomonitors to map atmospheric
mercury in a gold trade center city, Amazon, Brazil
Olaf MalmU , Marlon de Freitas Fonseca, Paula Hissnauer Miguel,
Wanderley Rodrigues Bastos, Fernando Neves Pinto
´ CCF 0 , Uni¨ . Federal do Rio de Janeiro (UFRJ), CCS, Ilha do Fundao,
Lab. Radioisotopos
EPF, Inst. Biofisica
´
˜ 21949-900,
Rio de Janeiro, Brazil
Abstract
Evaluation of Hg in urban air is a quite complex and expensive task since conventional sampling systems are
fragile and need special attention if long-term sampling is needed. Tillandsia usneoides, a Bromeliacea, is an epiphyte
that captures all its nutrients from the atmosphere, and concomitantly accumulates heavy metals, among them
mercury. Its morphology, with millimetric dimensions of the leaves and no roots, makes it ideal for handling and
preparation of transplanting systems and due to its high relation between surface area and mass, has a high efficiency
for Hg accumulation. One hundred systems of two baskets each with T. usneoides were distributed through Alta
Floresta city}MT and recovered after an exposure of 15 and 45 days during the dry season ŽAugust]September,
1995. and also repeated during the rainy season ŽFebruary]March, 1996.. Each compartment Žbasket. contained 5 g
of plants previously collected in a clean area. Only the younger parts were selected for transplantation experiments.
Systems were hung at 2]20 m height in open areas, close to and in the surroundings of the gold shops as well as in
control areas. Relative occupational exposure was also evaluated with systems installed inside gold dealer shops.
Concentrations of Hg in the exposed plants were remarkably high in the shops, reaching values up to 26 ppm Žparts
per million. or 300 times higher than in the control plants. Q 1998 Elsevier Science B.V.
Keywords: Mercury; Epiphyte plants; Tillandsia usneoides; Amazon, Brazil; Goldmining
1. Introduction
The Alta Floresta city}MT, in South Amazon
is 18 years old and had reached 350 000 inhabi-
U
tants during its first 14 years. The gold rush in
Amazon is now highly reduced by a factor of
3]10, and in Alta Floresta we suggest a reduction
from 6 to 8 and the city population is now also
reduced to 60%. After prospecting for gold with
amalgamation and burning the amalgam in the
field, a reburning process during commercialisa-
Corresponding author.
0048-9697r98r$19.00 Q 1998 Elsevier Science B.V. All rights reserved.
PII S0048-9697Ž98.00074-6
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
58
tion takes place in the gold dealing shops in the
cities. Despite the reduction in goldmining activities, the city has high levels of Hg in the environment mainly in soils and buildings but still routine emissions are contaminating air, occupational places and surroundings.
Evaluation of Hg in urban air is a quite complex and expensive task since conventional sampling systems are fragile and need special attention. If long-term sampling is needed, the difficulties are even greater.
In order to improve understanding of the behaviour of Hg in the atmosphere in a tropical
climate, the development of new techniques for
these evaluations is necessary. The use of plants
as air pollution indicators has been widely reported in the literature. A classical example is the
use of bryophytes to map atmospheric metal deposition in Denmark, Sweden, Finland and Norway ŽRuhling
et al., 1987; Steinnes, 1993.. How¨
ever species used for monitoring in temperate
climates are not always suitable for use in Brazil,
mainly because of their low resistance to desiccation.
The bromeliad Tillandsia usneoides ŽLinnaeus .
proved to be an efficient accumulator of atmospheric Hg in the surroundings of a chlor-alkali
plant ŽCalasans, 1994.. It had been previously
used in Brazil for the evaluation of fluoride in
rain water ŽStrehl and Arndt, 1989. and now is
being used for volatile metallic Hg due to
goldmining.
This investigation is part of a large project that
is being carried out in the same area regarding
atmospheric Hg where several groups are working
with different techniques on different aspects of
mercury dispersion and deposition.
v
2.2. Specific
v
v
v
Evaluate atmospheric Hg levels and dispersion in an urban area, inside but mainly in the
surroundings of the main sources, the gold
dealing shops.
Verify the accumulation of Hg by the biomonitor as a function of time, distance from the
source and height from the soil.
Map the concentrations of Hg in the atmosphere in the urban areas of Alta Floresta
city, trying to identify the effects of prevailing
winds as well as the influence of seasonal
changes on atmospheric Hg.
3. Biology of Tillandsia usneoides
T. usneoides presents CAM ŽCrassulacean acid
metabolism., opening the stomata predominantly
at night to avoid water losses. This tolerance to
hydric stress makes T. usneoides more appropriate than bryophytes or lichens for biomonitoring
tropical environments.
T. usneoides belongs to the Bromeliaceae
family, is a non-parasitic epiphyte that captures
all its necessary nutrients and water directly from
the atmosphere, therefore it is called an atmospheric bromeliad ŽBenzing and Renfrow, 1980..
Concomitantly with nutrients, it accumulates pollutants and heavy metals, including mercury. Its
morphology and physiology make it ideal for handling and preparation of the transplanting systems. Its other main characteristics are:
v
2. Objectives
2.1. General
Optimise the use of the biological monitor,
the bromeliad T. usneoides.
v
v
Its ramified morphology with millimetric dimensions provides a high ratio between area
and mass, and consequently a large number of
adsorption and or absorption sites. It has a
high efficiency for Hg incorporation Žor uptake. or bioconcentration capacity.
The presence of leaf scales controlling the
balance of water makes it ideal for hot climates.
It has a very slow growing rate Žrank vegetative growth., avoiding problems like growth
dilution factors.
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
v
v
It has no roots and lacks contact with the soil.
It is easily manipulated and transplanted.
4. Material and methods
One hundred systems of two baskets each with
T. usneoides were distributed through the city of
Alta Floresta}MT, two times during the year:
v
v
During the dry season ŽAugust]September,
1995. with average daily temperatures of
33]378C and;
During the rainy season ŽFebruary]March,
1996. with average daily temperatures of
27]318C.
Each basket Žmade of an inflexible plastic net
with 0.5 cm pores. contained around 5 g fresh
weight of plants previously collected in known
clean areas Žused during the last 5 years.. Only
the younger parts were selected for transplantation experiments ŽFig. 1.. Systems Žwith two baskets covered with a roof. were hung at 2]20 m
height in open areas, close to and in the surroundings of gold shops, inside them, as well as in
control areas. Relative occupational exposure was
also evaluated with systems installed inside gold
dealer shops. A shop that stopped operation was
evaluated after a 10- to 15-month break when the
area was being partially used for another purpose.
Fifteen and 45 days after distribution, plants
Fig. 1. Transplanting methodology used for biomonitoring
atmospheric Hg.
59
from one of the baskets of the system were collected and transported to the laboratory in closed
glass flasks. A total of 400 baskets was used in the
two transplant experiments, including several local control systems in Alta Floresta and Rio de
Janeiro.
Mineralisation of the plants for Hg analysis is
shown in Fig. 2 adapted from Calasans Ž1994..
Determination of Hg was done by Cold Vapour
Atomic Absorption Spectrophotometry ŽVarian
VGA-76 and AA-1475..
To complement this work, experiments with
closed systems with known atmospheres of Hg
have been running for the last 3 years with the
aim of calibrating the biomonitor. Preliminary
results are presented here.
To try to understand more about the dust and
its association with the plants after exposure,
different procedures with sonication and conventional washing ŽFig. 2. were performed with some
plants and Hg concentrations in the washing solution and particles were compared.
5. Results and discussion
Concentrations of Hg in exposed plants were
remarkably high inside the shops, or close to their
exhaust outlets reaching values up to 26 ppm or
300 times higher than control plants Žaround 80
Fig. 2. Mineralisation technique for Hg analysis in Tillandsia
usneoides.
60
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
Table 1
Average, minimum and maximum Hg concentration in Bromeliads from urban areas and inside goldshops in Alta Floresta; dry
season
Evaluated area
N8 of
systems
Average
Žppb.
Range
Žppb.
Very close to Hg emission sources Ž( 5 m.
Inside goldshops
Points close to shops Ždistance - 20 m.
Points far from shops Ž200 m- distance - 500 m.
Local controls in Alta Floresta Ždistance ) 1000 m.
Controls at Rio de Janeiro
2
12
34
27
14
3
12 185
4255
363
296
169
200
1895]22 480
550]26 775
- LD]2205
- LD]895
- LD]420
- LD]390
ppb, parts per billion; LD, detection limit Ž80 ppb..
ppb.. A decrease in Hg concentrations was
observed when moving away from the sources
Žgoldshops.. Tables 1 and 2 illustrate this in both
dry and rainy seasons. A clear seasonal trend with
higher values in the dry season is also seen in
Tables 1 and 2. This was observed mainly in
systems located outdoors but also inside the gold
shops. Indoor systems generally presented an average value three times higher during the dry
season compared with the rainy season, probably
reflecting the typical reduction of gold production
in the wet period. In the dry season, we observe
an average value nearly 12 times higher inside the
shops than in the surroundings Ž5]20 m. indicating that the critical areas are inside the goldshops
and in very close proximity. Results in Tables 1
and 2 are based on 45 days exposure.
The systems exposed inside the goldshop that
stopped operation showed reasonably high values
showing the importance of regulating future uses
of previous goldshops.
Fig. 3 illustrates the typical behaviour of Hg in
systems in locations close to goldshops Ždistance
5]20 m. as a function of height. Fig. 4 shows the
typical behaviour of Hg in plants inside the goldshops. Both of these figures are representative of
the average relations we obtained for concentrations after 15 and 45 days as well as the relation
between dry and rainy seasons.
The average increase of Hg found in systems
placed in the same sites from the rainy season to
the dry season was 246% Ž n s 32. considering
both 15 and 45 days exposure ŽTable 3.. Inside
the goldshops, this growth was 197% Ž n s 7. while
for outdoor systems the increase was 136% Ž n s
28., not including the closest points. This probably
reflects the reduction of gold commercialisation
in the goldshops but also could be related to the
association of Hg 0 with particulate matter which
is probably more important during the dry season
when the amount of dust in the air is also much
greater. The average daytime temperature is also
Table 2
Average, minimum and maximum Hg concentration in Bromeliads from urban areasand inside goldshops in Alta Floresta; rainy
season
Evaluated areas
N8 of
systems
Average
Žppb.
Range
Žppb.
Very close to Hg emission sources Ž( 5 m.
Inside goldshops
Points close to shops Ždistance - 20 m.
Points far from shops Ž200 m- distance - 500 m.
Local controls in Alta Floresta Ždistance ) 1000 m.
Controls at Rio de Janeiro
10
10
57
}
3
2
5245
1665
450
}
95
- LD
2510]9450
220]5255
105]1370
}
- LD]120
- LD
ppb, parts per billion; LD, detection limit Ž80 ppb..
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
61
Table 3
Percentage increase of Hg between rainy and dry seasons
Fig. 3. Mercury concentrations on biomonitors after 15 and
45 days exposure in the same place Žoutside goldshops. during
dry and rainy seasons. Representative case.
higher in the dry season. Points very close to the
goldshops showed much higher values during the
dry period.
As confirmation of the efficiency of atmospheric Hg uptake by plants, 10 of the 15 systems
which presented the highest values after 15 days
exposure also had the highest concentrations after 45 days exposure Ž67% correspondence. and
almost in the same order during the rainy season
Fig. 4. Mercury concentrations on biomonitors after 15 and
45 days exposure in the same place Žinside goldshops. during
dry and rainy seasons. Representative case.
Location
n
Increase Ž%.
General
Inside goldshops
Outside goldshops
32
7
28
246
197
136
ŽFig. 5.. This happens in the dry season ŽFig. 6.
with more agreement than in the rainy season
where 12 of the 15 were the same Ž80%.. This
confirms that for locations with higher atmospheric Hg, 15 days exposure was sufficient time
for a precise integration. A similar study in a
chlor-alkali plant in Rio de Janeiro, Brazil showed
7 days to be sufficient time for good integration
ŽCalasans, 1994..
Considering the total Hg found in all the systems after 45 days exposure, compared with 15
days exposure, we found a general average increase of 573% in the dry season and 183% in the
rainy season. Inside the goldshops, this percentage was quite similar for the two seasons: 224%
and 242% in the dry and rainy season, respectively, showing little influence of high humidity
and less dust in the air. In outdoor systems Ž) 20
m., this percentage was 184% and 146% in dry
and rainy season, respectively ŽTable 4..
During the rainy season, a relative increase of
Fig. 5. Comparison between 15- and 45-day sampling periods.
Relative to highest values in 45-day sampling. Rainy season.
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
62
Fig. 6. Comparison between 15- and 45-day sampling periods.
Relative to highest values in 45-day sampling. Dry season.
Hg in higher locations, in systems close to sources
were observed suggesting an easier dispersion of
free Hg 0 in those situations. Further away from
the sources, the 45-day exposure sampling period
is more representative. In the dry season, the
importance of the association of Hg 0 with particles is probably much more important.
The coefficient of variation between Hg concentrations in systems at the same location but
just different heights, decreases with distance from
the Hg sources ŽFig. 7.. This suggests more
sporadic events in systems closer to the sources.
Those events, like strong winds can cause resuspension of contaminated dust. The coefficient of
variation was twice as high during dry season.
Systems on trees at the same distance from the
sources showed higher levels than those suspended on lampposts ŽFig. 8.. Even at points far
Žaround 350 m. from the sources, we found high
values of Hg in a large tree situated after a
Fig. 7. Coefficient of variation of Hg concentrations in systems at the same point as a function of distance. Dry season.
deforested area and in the direction of the prevailing winds from the Hg sources. This suggests
that the vegetation acts as a barrier capturing Hg
and creating a more contaminated microsystem.
At the same points, we observe variation of Hg
in plants according to height. Considering points
with at least 3 to 6 heights, the occurrences of
highest concentrations were at 2.5 and 4.5 m in
the dry season ŽFig. 9. and 3.5 and 5.5 m in the
rainy season ŽFig. 10.. This suggests that transport
of Hg is being controlled by particles, more abundant in the dry season reducing the height of Hg
transport.
Table 4
Percentage increase of Hg between 15- and 45-day sampling
Location
General
Inside goldshops
Outside goldshops
Dry season
Rainy season
Increase
Ž%.
n
Increase
Ž%.
n
573
224
184
90
10
80
183
242
146
80
8
72
Fig. 8. Average concentration of Hg in systems at the same
point as a function of distance. Dry season.
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
Fig. 9. Occurrence of highest Hg concentrations as a function
of height. Dry season.
63
Fig. 11. Calibration of the biomonitor. Hg concentration in
the plant as a function of time. Average Hg levels in the air
Ž m g.my3 . up to each time are inside the rectangles.
6. Conclusions
Preliminary results obtained from the calibration of the plant ŽFig. 11. indicate that the Hg
concentration in the air of the shops would be
around 200 m g.my3 , in the same order of real
measured values from literature ŽMalm et al.,
1991..
Evaluation of dust washed off the plants Žsolution q particles. showed ŽFig. 12. different relative concentrations between downtown and a more
rural area and that sonication can remove significantly more Hg from the plant.
Fig. 10. Occurrence of highest Hg concentrations as a function of height. Rainy season.
Biological monitoring using bromeliads presents some clear advantages over traditional determinations with instruments:
v
v
It allows assessment of hundreds of sites at
the same time.
It integrates exposure over longer periods of
time, and to a certain extent solves a typical
problem of atmospheric studies, that of longterm sampling with more representative samples.
Fig. 12. Relative Hg concentrations in dust adsorbed to plants
from different sites, removed with different washing procedures.
O. Malm et al. r The Science of the Total En¨ ironment 213 (1998) 57]64
64
v
v
It has a very low cost.
It gives an idea of bioavailability.
A clear seasonal difference was observed
probably due to reduction of the goldshops’ activities. Dust, temperature and humidity of the air
probably have a strong influence over Hg atmospheric transport.
As a recommendation concerning previous
goldshop workplaces, attention should be paid to
future uses of these stores since the one studied
showed high levels even after a 15-month interruption to activities. If the place is being used as
a closed shop with air conditioning, values can get
even higher.
A more detailed statistic approach with modelling of the data is under preparation.
Acknowledgements
Financial support for this study was from CNPq,
FINEP, FUJB and UFRJ.
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