Atmospheric Pollution in a Tropical Rain Forest: Effects of Deposition Upon Biosphere and Hydrosphere II. Fluxes of Chemicals and Element Budgets

ATMOSPHERIC POLLUTION IN A TROPICAL RAIN FOREST:EFFECTS OF DEPOSITION UPON BIOSPHERE AND HYDROSPHERE

II. FLUXES OF CHEMICALS AND ELEMENT BUDGETS

ROBERT MAYER1, SIEGFRIED LIESS1, MARCIA INES MARTIN SILVEIRALOPES2 and KARIN KREUTZER1

1 Fachbereich 13, FG Landschaftsökologie/Bodenkunde, Universität Gh Kassel, Gottschalkstrasse28, D-34109 Kassel, Germany;2 Instituto de Botânica, Caixa Postal 4005, CEP 0106-970 São

Paulo, SP, Brazil

(Received 23 February 1999; accepted 16 August 1999)

Abstract. Three rain forest ecosystems in the Serra do Mar, the atlantic coastal mountain rangeof Brazil, have been investigated in the frame of an interdisciplinary German-Brazilian researchproject on dispersion, transformation and deposition of air pollutants in and around the industrialarea of Cubatão. Part I of this paper gives a description of the overall goals of the project, the area ofinvestigation, and the materials and methods used. It reports on the results of the field measurementsconducted from 1991 to 1995, covering concentrations of chemicals in precipitation, soil water,surface water and litter fluxes. In the present paper, part II, the element fluxes are presented withcalculated concentrations in the transport media (precipitation, seepage water, litterfall) and theirrespective flow rates. Element budgets for the ecosystem and for the soil compartment are interpretedwith respect to turnover of chemicals, including nutrients, in forest vegetation, and to processes ofsoil acidification. The forests under investigation are characterized by a very high input from theatmosphere. Between 100 and 200 kg S ha−1 are annually carried into soil by precipitation in theform of sulfate, 20 to 70 kg of nitrogen mainly in the form of ammonium, 3 to 24 kg of fluoride.Input of ammonium and organic bound nitrogen is followed by nitrification in the top soil. At themost polluted site, nitrate output with seepage amounts to 300 kg N ha−1 yr−1, sulfate output tomore than 400 kg S. Soil acidification associated with turnover of sulfur and nitrogen is followed bythe release of aluminum from soil minerals, and leaching of ionic forms of Al (up to 280 kg Al ha−1

annually). Transfer of aluminum ions to groundwater and surface water can have serious ecologicaleffects. Alkalinity is consumed, and the water is subject to acidification.

Keywords: acidification, air pollution, atmospheric deposition, Brazil, Cubatão, element fluxes,element budgets, Serra do Mar, tropical rain forest

1. Introduction

The overall goal of the interdisciplinary German-Brazilian research project was toassess dispersion of pollutants, their deposition in the region surrounding the indus-trial complex of Cubatão, and to provide damage evaluation and risk assessmentwith respect to forest vegetation, soils and hydrosphere. The part of the sub-project‘Soil Module’ was the assessment of atmospheric deposition to forest ecosystemsat a few selected sites representing local pollution situations. In ecosystem stud-ies, the fluxes of chemicals going into the system, and leaving it, as well as the

Water, Air, and Soil Pollution121: 79–92, 2000.© 2000Kluwer Academic Publishers. Printed in the Netherlands.

80 R. MAYER ET AL.

transfer fluxes between single compartments are usually not accessible for directassessment. In experimental ecology the following method of flux assessment iswidely applied: element concentrations are measured in the flow medium, in whichthe transfer takes place. These are, e.g., precipitation and seepage water, litterfall,sediment transport. Simultaneously the flux of the flow medium is determinedfor a defined time period, and element fluxes are calculated as the product ofconcentration and flux of the medium. The concept was developed and used inseveral countries in the frame of the International Biological Program (Ellenberg,1971). The present study follows this concept. Besides the litter turnover of forestvegetation, the main fluxes are those associated with water, the flow rates beinginterrelated by the ecosystem water balance equation.

2. Water Balance

The complicated structure of the ecosystems under investigation, situated on thesteep southeastern slopes of the Serra do Mar, made an assessment of evapotran-spiration fluxes and soil water fluxes a too difficult task to be solved in the frame ofthis program. With regard to the research goals, as described in Part I of this paper,a good estimate of actual water fluxes, based upon measured precipitation on eachsite, seemed to be sufficient for the purpose of showing the impact of air pollutionunder different pollution loads.

There are several methods to estimate potential and actual evapotranspirationfor a given area when precipitation data and other meteorological parameters areavailable. In the present study we relied upon the data from Setzer (1976) whopublished isoline maps of effective evaporation for the Serra do Mar, including theproject region, based upon a large number of meteorological stations in the Stateof São Paulo. Setzer has shown that standard calculation models for evapotran-spiration are not applicable for the Serra do Mar, because they are not adapted tothe perhumid climate and the frequency of clouds in the upper mountain regions.Therefore they lead to overestimate evapotranspiration and, as a consequence, un-derestimate surface and subsurface runoff. Evaporation data from Setzer (1976) ap-ply to a ‘normal’ year, with an average precipitation and temperature regime. In ourstudy, we used evaporation percentages from Setzer to estimate actual evapotran-spiration from monthly precipitation values in open field, adjusted for losses frombulk samplers by comparison with wet-only samplers of the chemistry module.Evapotranspiration from soil at different depth levels was estimated by partitioningtotal actual evapotranspiration according to root density observed in the soil profile.The annual water balance for the sites, averaged over the period 1991–1995, isgiven in Table I.

Interception percentages of 5 to 7% are also reported from perhumid rain forestin Venezuela by Jordan and Heuveldop (1981) and from amazonian rain forestnear Manaus/Brazil by Lloyd and de O. Marques (1988). A small fraction of the

ATMOSPHERIC POLLUTION IN A TROPICAL RAIN FOREST 81

TABLE I

Annual average water balance (1991–1995)

L (m2∗a)−1 Pilões Mogi Paranapiacaba

Precipitation open fielda (= input) 2712 2609 2883

Precipitation below canopy 2563 2466 2724

Soil water flux 10 cm depth 2335 2246 2573



a Adjusted for evaporation losses from bulk samplers.

rain reaches ground by stem flow. This flux has only been sampled during the initialphase of investigations, because the difficulty of collection along the very spiny andirregular stems of the dominant palm species was considerable. This seemed to bejustified in view of the very small amount of stemflow found, and it is supported byother authors like Whitmore (1990) who estimate this flux in most tropical foresttypes to be less than 5% of precipitation below canopy. Percentages of 1 to 2% arereported for primary rain forests in the States of Amazonia, Pará, and Rondônia(Lloyd and de O. Marques, 1988; Ubarana, 1995).

Characteristics of the perhumid climate in the Serra do Mar, with high rates ofprecipitaion (P) and seepage (S) and small rates of evapotranspiration/interception(ETI), are revealed by Figure 1, in which Paranapiacaba is compared with a sec-ondary growth forest (humid tropical) in the State of Pará (Hölscher, 1995), and aspruce forest (temperate climate) in Solling/Germany (Ellenberget al., 1986).

3. Results

3.1. ELEMENT FLUXES ASSOCIATED WITH PRECIPITATION ABOVE AND

BELOW VEGETATION CANOPY

Table II gives the depositon rates associated with precipitation above and belowcanopy. The fluxes have been calculated by multiplying the ionic concentrationsmeasured in the liquid phase with the respective amount of water per unit timeand area (water flux). Although there are only small differences in the amount ofprecipitation, the element fluxes differ considerably between investigation sites.For all components except K and Al, the highest input with open field precipitationis found in Mogi.

Flux rates increase considerably during canopy passage for most elements in-vestigated. Only ammonium shows little change of flow rate, and protons tend tobe reduced as a consequence of buffering reactions.

82 R. MAYER ET AL.

Figure 1.Water balance for three forest ecostems in tropical and temperate climates (after Hölscher,1995 and Ellenberget al., 1986).

3.2. ELEMENT FLUXES ASSOCIATED WITH SEEPAGE WATER

Estimates for element fluxes across different depth levels of the soil profile havebeen gained by multiplying seepage water fluxes with ionic concentrations in soilsolution, extracted in the respective depth by use of ceramic cups (see part I of thispaper). Results are listed in Table III.

Due to the perhumid climate, seepage water fluxes are very high, compared totemperate climates. The element fluxes, therefore, are also much above the flowrates found elsewhere although concentrations in soil water are not excessivelyhigh.

Fluxes in Mogi are extremely high for nitrate, sulphate and aluminium. In Pilões,nitrate fluxes decrease with soil depth, while in Mogi they remain fairly constanton a much higher level.

3.3. DEPOSITION WITH LITTERFALL

In addition to the ionic load of precipitation below the canopy, forest floor receivesan input of chemicals – pollutants as well as plant nutrients – associated with lit-terfall. After decomposition and mineralization of the litter, dissolved components


TABLE II

Deposition with precipitation (Annual average 1991–1995)

Deposition with precipitation Pilões Mogi Paranapiacaba

(g (m2∗a)−1)

NO3-N open field 0.66 1.03 0.66

below canopy 1.29 1.48 0.76

SO4-S open field 4.09 11.04 5.61

below canopy 9.85 21.32 9.99

F open field 0.29 1.47 0.46


Cl open field 6.63 7.39 4.65

below canopy 11.52 14.55 9.03

K open field 1.07 1.93 2.73

below canopy 13.20 8.01 7.85

Na open field 3.13 3.26 1.95


Mg open field 0.34 1.64 0.38


Ca open field 1.33 7.63 2.75

below canopy 4.04 15.46 6.55

Al open field 0.18 0.18 0.52


NH4-N open field 0.52 4.25 1.33


H open field 0.136 0.224 0.032

below canopy 0.025 0.040 0.036

enter into the liquid phase of mineral soil. From here they may return to vegetationby root uptake (internal cycling), be adsorbed by the mineral phase or by soilhumus, or they may be leached to deeper soil layers with seepage.

Annual averages of dry weights and element fluxes associated with litterfall aregiven in Table IV. Pilões showed the highest production of litter, followed by Mogiand Paranapiacaba. The leaf fraction came up for about 70 to 75% of total litterproduction.

84 R. MAYER ET AL.

TABLE III

Soil water fluxes in different depths (annual average1991–1995)

Depth Pilões Mogi Paranapiacaba

(g (m2∗a)−1)

NO3-N 10 cm 7.33 32.89 2.65

60 cm 2.08 29.53 2.08

100 cm 1.55 30.02 1.62

SO4-S 10 cm 9.99 40.30 14.54

60 cm 8.26 52.06 10.96

100 cm 7.59 42.12 10.01

F 10 cm 0.37 2.49 0.51

60 cm 0.32 3.15 0.51

100 cm 0.48 2.04 0.35

Cl 10 cm 11.98 23.16 5.76

60 cm 9.87 17.97 5.67

100 cm 9.25 11.92 5.21

K 10 cm 5.18 4.09 0.33

60 cm 2.54 0.69 0.25

100 cm 0.91 0.55 0.30

Na 10 cm 7.57 13.01 3.55

60 cm 5.05 5.13 2.64

100 cm 4.72 4.10 2.07

Mg 10 cm 5.79 9.32 0.59

60 cm 3.51 4.64 0.20

100 cm 3.28 3.73 0.13

Ca 10 cm 5.79 25.90 1.62

60 cm 2.42 7.06 0.71

100 cm 1.66 9.64 0.56

Al 10 cm 1.91 14.96 2.65

60 cm 1.52 25.52 4.09

100 cm 0.84 28.64 4.35

NH4-N 10 cm 0.23 0.45 0.21

60 cm 0.18 0.22 0.20

100 cm 0.18 0.24 0.20

H 10 cm 0.071 0.580 0.566

60 cm 0.068 0.400 0.456

100 cm 0.035 0.350 0.332


TABLE IV

Deposition with litterfall (annual averages1991–1994)

Litterfall Pilões Mogi Paranapiacaba

(g (m2∗a)−1)

Dry weight 943 894 789

N (total) 16.08 16.77 15.71

S (total) 1.81 1.93 1.63

P (total) 0.60 0.91 0.75

K 2.98 1.41 1.78

Ca 10.04 9.67 10.52

Mg 2.18 1.11 1.40

Na 1.77 1.52 1.56

B 0.04 0.03 0.03

Cu 0.01 0.01 0.01

Fe 0.76 2.41 1.61

Mn 0.51 0.13 0.28

Zn 0.04 0.04 0.04

4. Discussion

4.1. FLUXES ASSOCIATED WITH PRECIPITATION

More than 200 kg ha−1 of S (in the form of sulfate), 70 kg of nitrogen (as am-monium and nitrate), 24 kg of fluoride are annually carried into soil at the Mogisite by precipitation. Compared with other regions of the tropical and temperatezone, this site represents, during the period 1991–1995, the most polluted forestecosystems with respect to the components considered.

Atmospheric input of potassium at the three sites is higher than usally foundin european forest ecosystems, possibly due to emissions from fertilizer industry.Extremely high K fluxes are associated with throughfall precipitation. They maybe caused by anthropogenic emissions, but there are investigations in undisturbedtropical rainforests in Panama (Jordan, 1985) and New Guinea (Whitmore, 1990),which showed similarly high K fluxes in throughfall. Probably, internal cyclingand leaching potential of potassium in tropical trees and epiphytes, under perhumidconditions, are more intensive than in temperate forests.

86 R. MAYER ET AL.

4.2. FLUXES ASSOCIATED WITH LITTERFALL

Fluxes associated with litterfall account, at all investigated sites, for less than 20%of S and K input to soil. In contrast herewith, the soil input of Ca and Mg associatedwith biogenic turnover amounts to 40 to 60%. The input of Ca and Mg with litterfallin temperate forest ecosystems is much less than in the investigated tropical forests(about 7 to 10 times) but comparable to other tropical regions (Grubb, 1995). Inthe case of nitrogen, litterfall is the dominant type of element transfer in nutrientcycling, accounting for 60 to 90% of soil input.

4.3. FLUXES ASSOCIATED WITH SOIL WATER

At the Mogi site, a high input of ammonium, being transformed into nitrate in thesoil (nitrification), washed out to a large extent beyond the level of 100 cm, indicat-ing that the nitrogen cycle is far from being closed. In contrast to this, at Pilões andParanapiacaba most of the nitrogen carried into the ecosystem is taken up by roots,together with the nitrogen mobilized by mineralization of organic matter. The largeamount of ammonium, deposited by precipitation to the Mogi site, is converted tonitrate, a process generating acidity, thus increasing soil acidification.

High deposition rates of calcium and magnesium at the Mogi site cannot com-pensate for the loss of bases even in the deeper subsoil, for these cations arestrongly leached from soils due to acidification. Potassium is an essential nutrientand strongly adsorbed by plants, therefore the rate of loss by seepage is relativelysmall.

Chloride ions are very mobile, and usually are not adsorbed by soil minerals toany degree. The decrease in chloride flux with increasing soil depth, as observedin Pilões and Mogi, must therefore be explained by internal cycling of Cl, i. e.uptake by roots, transfer to the canopy with transpiration flux, and leaching fromthe canopy by precipitation, or return to forest floor with litterfall.

4.4. ELEMENT BUDGETS

The net balance of element fluxes for ecosystem compartments is calculated asdifference between input to and output from the system. In Figures 2–5 the elementbudgets of S, N, and Al are visualized by showing element input (positive) withprecipitation below canopy together with output (negative) by seepage water. Inorder to put the results of our investigations into a frame with results from otherregions, fluxes at Mogi are compared with data from an unpolluted secondarygrowth tropical forest in the northern part of Pará, Brasil (Igarapé Açu; Hölscher,1995), and from a temperate spruce forest in Central Europe (Solling/Germany,after Ellenberget al., 1986) with relatively high pollution.

Soil input of nitrate with precipitation in Mogi (14.8 kg N ha−1 yr−1) – abouttwice as high as in Paranapiacaba – is of the same magnitude as in the european


Figure 2.Nitrate balance.

Figure 3.Ammonium balance.

88 R. MAYER ET AL.

Figure 4.Sulfate balance.

Figure 5.Aluminium balance.


spruce forest (15.5 kg N ha−1 yr−1). In contrast to this, in Igarapé Açu there is nomeasurable input of nitrate.

The extraordinary situation in the Serra do Mar becomes obvious with regard tonitrate output with seepage (300 kg N ha−1 yr−1). It exceeds the input by a factor20, while, on the other hand, the output in Solling and Igarapé Açu amounts toless than 2% of input. The soil in Mogi acts as source for nitrate, and comparisonwith the ammonium balance shows that output of nitrate by far exceeds the inputof ammonium. Therefore, we must assume that ammonium which is depositedfrom the atmosphere, is readily transformed into nitrate (nitrification), which isthen lost from soil by seepage. In addition to this, mineralization of nitrogen boundin organic matter contributes to the nitrate load of seepage water, nitrogen storesin humus being depleted. It is interesting to note that the loss of nitrogen withseepage is almost twice as high as the flux associated with litterfall (Table IV).From european land use history we know about the devastating effects of litterexport with respect to the nutrient status of soils.

The element budget for ammonium is closely related to the nitrate budget. Theinput is very high in Mogi (5.58 kg N ha−1 yr−1), about 7 times as much as inPilões, and 3 times as much as in the Solling. Again, the input of ammonium inIgarapé Açu is below the detection limit. In spite of large differences in the input,all sites have in common that the output of ammonium with seepage is very low.Ammonium is either retained by soil minerals, taken up by plants or, as shownin the case of Mogi, it is transformed to nitrate and then subject to loss from soilwith seepage. It was already pointed out, that this process produces an equivalentamount of acidity, thus contributing to soil acidification and loss of nutrient cations(like Ca, Mg, K).

The sulfate balance is shown in Figure 4. The Solling spruce forest (85 and40 kg S ha−1 yr−1 for input and output, respectively) must be considered, in com-parison with european pollution surveys, as highly polluted with respect to atmo-spheric sulfate. Even here the Mogi site is far ahead, with 213 and 421 kg S ha−1

yr−1 for input and output, respectively. In contrast to this, sulfate deposition andseepage water output are almost negligible in Igarapé Açu (5 and 0.9 kg S ha−1

yr−1). The sulfur balance at the Mogi site is negative, i.e. there is a net loss of sulfatefrom soil, soil acts as a source. Obviously, the capacity of the mineral soil to retainsulfate is exhausted. In contrast to this, in Paranapiacaba input and output ratesare almost the same, while in Pilões, the less acidified site, leaching is lower thandeposition with precipitation. Here, the mineral soil is still able to retain sulphate.

The aluminum balance is shown in Figure 5. While there is almost no turnoverof aluminum in Igarapé Açu, both at the Mogi site as well as in Solling a smallinput goes together with a large output. The rate of output in Mogi is consider-ably higher than in the Solling (286 vs 52 kg Al ha−1 yr−1). These figures reflectthe rate by which soil acidification is taking place at these sites, since aluminumwashed out with seepage is released from soil minerals by consuming protons from

90 R. MAYER ET AL.

soil solution. Aluminum ions entering groundwater and surface water, lead to aconsumption of alkalinity, and to water acidification.

In order to evaluate the actual turnover of elements with respect to soil devel-opment, it is of interest to compare the flux balance with the element stores of themobile fraction in mineral soil (Part I of this paper, Table II). The soils stores are,compared with turnover fluxes, almost negligible or small for Na and K. In view ofplant nutrition, the situation with respect to K is alarming, for mineral soil containsalmost no reserves in this nutrient element. The situation is similar for Mg and Ca,especially at the Mogi site. On the other hand, the stores of aluminum, a potentiallytoxic element when it goes into solution in ionic form, is huge, essentially infinitewith regard to ecosystem life cycles.

In the unpolluted area of Igarapé Açu the Ca and Mg deposition rates are abouthalf of those at Pilões, the reference site in this project. There is a clear relationbetween deposition rates and distance from emission sources (Pilões< Paranapi-acaba< Mogi). In Pilões and Igarapé Açu the input/output-budget for calcium isalmost balanced. Although there is a high Ca deposition with precipitation in Mogi,due to the very acid conditions, where the exchanger is occupied by Al3+, calciumis not retained.

In Paranapiacaba the soil acts as a sink for Ca. But in spite of this the stores ofexchangeable calcium in the mineral soil of Paranapiacaba and Mogi are very low(11.4 and 2.8 keq ha−1, respectively) compared to Igarapé Açu (64 keq ha−1), andSolling (9 keq ha−1). While soils poor in nutrients are quite common in tropicalregions (Jordan, 1985), the sites of the Serra do Mar represent some of the lowestnutrient levels in this spectrum.

Cycling of sodium in ecosystems is similar to that of potassium, but it is seldommeasured on an ecosystem scale because it rarely appears to limit plant growth.Near the coast potassium and chloride are deposited in high amounts (seaspray).The same is observed in the Wingst area (Northern Germany, Büttner, 1992). InParanapiacaba and Pilões, input and output rates of fluoride are almost the same.In Mogi, the heavily polluted site, the soil acts as a sink.

5. Conclusions

Summarizing the results of the study we conclude that deposition of atmosphericpollutants to the Serra do Mar shows a very heterogeneous distribution over theland surface. Deposition rates measured at three sites are in good agreement withthe results from the Transport and Chemistry Modules: Observation of wind fieldsand calculation of deposition patterns by use of transport models (Fiedler andMassambani, 1997) showed deposition rates of SO2 in the Mogi area to be 2 to5 times higher than at the southwestern site (Piloes) and at the rim of the plateau(Paranapiacaba). Independent observations and model calculations on wet and oc-cult deposition (Jaeschke, 1997) showed similar relations for sulfur and nitrogen


compounds, and cloud water droplets deposition turned out to play a secondaryrole, less than 10%, compared to deposition with rain. In our study we were able toshow that soils are affected mainly by the input of nitrogen compounds and sulfate,but also by fluoride. The negative effects to the ecosystem, depending upon themagnitude of deposition rates of pollutants, is seen in:

• soil physico-chemical conditions, like low pH, acidification of exchange com-plex• an increase of soil internal acid production by mineralization of organic matter

and nitrification• degradation of vegetation due to direct effects to the forest canopy, low sup-

ply of nutrients and/or disequilibrium in nutrient supply. Degradation causesfurther nutrient losses, for forest vegetation with undisturbed soil organismsacts as an important motor for storage and recycling of nutrients, which keepselement cycles closed and prevents leaching losses• the transfer of acidity from soil to hydrosphere• an acceleration of nutrient turnover (N, S, Ca, Mg, S) with loss of nutrients

from soil/ecosystem to hydrosphere

The results are a good base for comparison with conditions in other ecosystems, aswell as for monitoring of changes in environmental conditions of the area.

Acknowledgements

This project was carried out within the scope of the Agreement on Cooperationin Scientific Research and Technological Development signed by the German andBrazilian governments, and within the Project Agreement of GKSS/Germany andSMA/Brazil.

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Ellenberg, H. (ed.): 1971,Integrated Experimental Ecology, Springer Berlin, Heidelberg, New York(Ecological Studies2), 214 p.

Ellenberg, H., Mayer, R. and Schauermann, J. (eds.): 1986,Ökosystemforschung – Ergebnisse desSolling-Projekts, Verlag Eugen Ulmer, Stuttgart.

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– the Serra do Mar as an Example, Final Report, Dortmund/São Paulo SMA/Geesthacht GKSS.Lloyd, C. R. and de O. Marques, A.: 1988,Agric. For. Meteorol.42, 63.Prenzel, J.: 1982,Ein bodenchemisches Gleichgewichtsmodell mit Kationenaustausch und Alumini-

umhydroxosulfat, Göttinger Bodenkundliche Berichte,72.Setzer, J.: 1976,Atlas de Evapotranspiração Efetiva no Estado de São Paulo, São Paulo, CTH.Ubarana, V. N.: 1995, Observation and Modelling of Rainfall Interception in Two Experimental Sites

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Documents

Atmospheric Pollution in a Tropical Rain Forest: Effects of Deposition Upon Biosphere and Hydrosphere II. Fluxes of Chemicals and Element Budgets