The fate of trace metals in suspended matter in a mangrove creek during a tidal cycle

The Science of the Total Environment, 75 (1988) 16~180 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

169

THE F A T E OF TRACE M E T A L S IN S U S P E N D E D M A T T E R IN A M A N G R O V E CREEK D U R I N G A T I D A L CYCLE

L.D. LACERDA 1, L.A. MARTINELLI 2, C.E.REZENDE 1, A.A. MOZETO 3, A.R.C. OVALLE 1, R.L. VICTORIA 2, C.A.R. SILVA 1 and F.B. NOGUEIRA 3

1Departamento de Geoqu$mica, Universidade Federal Fluminense, NiterSi, 24210 R J (Brazil) 2CENA, Universidade de $5o Paulo, Piracicaba, 13400 SP (Brazil) 3Departamento de Qu$mica, Universidade Federal de $5o Carlos, $5o Carlos, 13560 SP (Brazil)

ABSTRACT The variation of heavy metal content in suspended matter (SM) during tidal cycles in a mangrove creek is described. The stable isotope of carbon was used as a tracer for sources of SM to the system. During tidal cycles three patterns of metal variability were found. The first, represented by Fe, showed an irregular and small variability throughout the cycle; a second, represented by Mn, exhibited a sharp increase in concentration during the rising tide, coincident with the greatest variation of pH and E h. The third pattern, including Cu, Cd, Pb, Ni, Cr and Zn, showed maximum concentration at the peak of the high tide, coincident with a shift in SM source. The stable isotope of carbon indicated that, during low tides, most of the organic carbon exported originated from mangrove plant detritus, while during the high tides organic carbon imported by the system was almost totally of marine origin. This shift of SM source is the principal parameter controlling metal fluxes through the system. Changes in water pH and Eh, and manganese precipitation, can also serve as a secondary control. Although the results strongly suggest that the metallic load of marine SM is being immobilized by the mangrove environment, mass balance studies are necessary to show whether a net accumulation of metals is actually occurring. INTRODUCTION

Mangrove forests are the dominant vegetation form along most tropical shores, and their ecological importance to coastal areas is extensively documented, particularly as a source of organic matter to marine food chains (Heald, 1969; Boto and Bunt, 1981). The recent industrial development of various tropical regions, however, has become a potential threat to mangrove ecosystems and the fisheries they support (Lacerda, 1984; Odum, 1984). Among the many pollutants, by-products of industrialization, heavy metals have received special attention due to their long lasting toxicological effects and intensive accumulation in protected coastal zones and estuaries, where mangroves are best developed (Banus, 1977; Harbison, 1981; Lacerda and Rezende, 1984; Lacerda et al., 1986a). The role of mangrove forests in heavy metals cycling in coastal zones is poorly known. However, from the results obtained in temperate salt marshes (Lacerda et al., 1979; Gallagher and Kibby, 1980; Giblin et al., 1980; Nixon, 1980), two hypotheses can be advanced: (a) mangroves may be long-term sinks

0048-9697/88/$03.50

© 1988 Elsevier Science Publishers B.V.

170

for metals, by immobilizing them in sediments, consequently decreasing environmental risk; or (b) deposited metals may be remobilized through plant uptake and eventually exported with plant detritus, increasing the possibility of metals entering coastal food chains. Both hypotheses have been proved to occur in temperate salt marshes and in a few tropical areas, but the dominance of one over the other seems to be dependent upon local environmental characteristics and metal species (Nixon, 1980; DeLaune et al., 1981; Lacerda and Abr~o, 1984; Woodroffe, 1985b, c; Harbison, 1986). The balance between inputs and outputs of metals in estuarine areas is mostly dependent on the balance of the suspended matter (SM) load and its metal content (Jouaneau et al., 1983; Salomons and FSrstner, 1984), and this is also true in areas dominated by mangrove ecosystems (Lacerda and Rezende, 1984; Adaime, 1985). Therefore, the characterization of SM during tidal cycles is essential for the understanding of metal balances in mangrove ecosystems. This characterization must include not only the metal concentration in SM and the causes of their variability, but also the sources of SM to and from the mangrove ecosystem. The present study reports on the heavy metal content of SM during tidal cycles in a mangrove ecosystem. It also reports, by using the stable isotope of carbon, on the different sources of SM, and the abundance of metals in the system and of their variability during the tidal cycle. Due to the intrinsic variability of SM export from mangrove areas (Adaime, 1985; Woodroffe, 1985c) a mass balance of trace metal flux in these ecosystems is a long-term study entailing difficult logistics and will not be presented here. MATERIALS AND METHODS

The work was carried out on a mangrove forest at Sepetiba Bay, a moderately polluted coastal water body 80 km south of Rio de Janeiro city. The fate of metallic pollutants in the bay has been extensively studied (see Lacerda et al., 1983, 1985; Fiszman et al., 1984; Pfeiffer et al., 1985; Lima et al., 1986 for further details). The forest is a pure stand of red mangrove, Rhizophora mangle L., growing along a tidal creek which drains an area of ~ 4 ha (Fig. 1). Freshwater inputs are solely due to subsurface flow, minimizing the influence of terrestrial sources of SM (see 180/1~O data). A fixed sampling station was established at the mouth of the creek. Owing to the physiographic conditions of this basin, this single point approach would be sufficient to represent the quasi totality of SM balance through the area (see Woodroffe, 1985a, b, for a discussion of such an approach). Measurements of major physico-chemical parameters of the water (temperature, salinity, pH and Eh), current velocity and SM load, and water sampling were performed at 30 min intervals during high flow periods and at 1 h intervals during low flow periods, for two consecutive tidal cycles (25 and 26 February 1986). A third cycle (25 April 1986) was monitored at 20 min intervals to study variations in pH and Eh.

171 ~s~yRIO

.

DEJANEIRO STATE Aroo

l |N ~

~

Study Areo

SEPET/BA

BAY

Fig. 1. Map showing location of the area studied and sampling point. Current velocity was measured ,--40cm above the creek bed by a current meter attached to a pole. Water salinity, temperature, pH and E h were determined directly in the field by a portable salinometer and electrodes. Suspended matter load was measured by filtration of 0.51 of water through pre-weighed 0.45 pm pore diameter Millipore filters, while SM for metal determinations was obtained by decanting (for 2-16 h) and further filtration of 3-51 water samples through the same type of filters. This sampling procedure does not affect the metal content of SM; details can be found in J o u a n e a u et al. (1983). All direct measurements and water and SM sampling were carried out simultaneously. Water and SM samples of the mangrove and of the bay were also collected for the determination of the stable isotope compositions of oxygen and carbon. Both isotopes have been reported as consistent tracers of SM and water sources in this mangrove area (Lacerda et al., 1986b). The sampling procedure for '3C determination in SM was the same as described above for metal determination, with the exception t h a t filtration was performed with pre-combusted glass fiber filters. All metal determinations were carried out using conventional flame atomic absorption spectrophotometry, after total digestion of SM samples in a strong acidic mixture (conc. HC1/conc. HNOJconc. HClOt) (3:1:1) at 100°C on a hot plate (Fiszman et al., 1984). Stable isotope concentrations were determined by mass spectrometry. Samples for isotopic analysis were prepared by combustion of the filter with pre-combusted CuO in sealed, evacuated Pyrex break-seal tubes. The samples were combusted overnight at 550°C and purified by passage through alcohol~lry ice and liquid nitrogen traps. The stripped and purified CO2 sample was collected in a tube under liquid nitrogen in a high vacuum line. All 513C values are reported relative to PDB limestone (standard).

172

13c = [(13C/12C) "mP'e L

~_1 x

103

(1)

Analyses were performed using a MICROMASS model 602 E mass spectrometer fitted with a double inlet and double systems for simultaneous determination of 13C/12C and 180/160 ratios. RESULTS

Physico-chemical properties of creek water during the tidal cycle The current velocity of creek water during tides is shown in Fig. 2. Maximum velocity (170 cm s 1) was reached ~ 2 h after the inversion of the tide and lasted for ~ 1 h. Although the measurements could only be made during one tidal cycle, we believe they represent the general trend in tidal creeks in these mangroves, since the pattern is similar to various cycles monitored by Adaime (1985) in similar areas in S~o Paulo State, Brazil, and by Woodroffe (1985a, b) in a New Zealand mangrove forest with identical physiography as the studied area. The variation of the physico-chemical parameters determined is presented in Fig. 3 for the two cycles monitored. Figure 4 shows a detailed (every 20min) monitoring of water pH and redox potential (Eh) variation during the tidal cycle of 25 April 1986. Temperature was very high during the whole cycle, varying from 25.5 to 32°C. All measured parameters have the same pattern of variation during the two tidal cycles, therefore we will only report on the general pattern of variation. At the peak of low tide, salinity attains its maximum value (Fig. 3), while pH and Eh are at a minimum (Fig. 4). As the tide rises, salinity decreases slightly (Fig. 3), becoming almost constant until the peak of high tide. Redox potential

fo\

DAY 26•02/86 cm.s-I 160 120 _z 80 40 0 40

O

\

%20

E3

160 II

12

13

14

15

16

17

18

19

t(h)

Fig. 2. W a t e r c u r r e n t v e l o c i t y (cm s-2) of t h e s t u d i e d c r e e k d u r i n g one tidal cycle.

173 '%/'% DAY 26102/86

-0.8

0

-0.7

S%o

0 - -

Q. -0.6 - 0.5

211 19

- 0.4

17

-03

I5

-0.2

I3

_

_ ~ _

•_.

_-

• "0"~- / f

~ o

0~

.

.

25

-05

23

.....

Solmity

.

"'...

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

.."

:" ----_'"" --- -" Q ' "

/ o

/

Depth

0 ~°

.o: " - -/'o

(m)

i

""O. o

"'0

~ o ~

-0.1 II 180/160 S % 0 - -0.7 -06

0

.... Del~h {3----~ 18o/16o

""

sO~ty Depth

0-...0'%%

"..

~.o

05

o--o .....

D .. ° '° 0

1.5

.P

(m)

-0.4

:.0

-03 -0.2

,,

-0.1

15

..........

x ;-j

__ - - - ~

0 @ 0

o

1

""

,o 0.5

,

II

,

,

12

,

13

,

14

,

I.~

16

,

17

,

18

,

19

Fig. 3. Salinity, depth and lsO/l°O ratio variations during two tidal cycles. DAY 25/04/86

Eh(mV) 230

/0\ -0kO--

0~0\

2~0 190

/

o

0

O - - 0 Eh(mV) ~ - - 6 pH

o/

Depth (m)

#H

/0

170 80! o

150 75 t

'° II

125 O5

~b

.

~2

J',*

J'5

1'6

~'7

~8

tlh)

Fig. 4. Detailed (20-min intervals) variation of pH and Eh of creek water during one tidal cycle. and pH r e a c h their m a x i m u m v a l u e s at t h e p e a k o f t h e high tide, c o i n c i d e n t w i t h t h e i n c r e a s i n g c u r r e n t v e l o c i t y , and r e m a i n c o n s t a n t . H a r b i s o n (1986) reported similar b e h a v i o u r of w a t e r redox p o t e n t i a l in a m a n g r o v e in A u s t r a l i a . Therefore, m o r e o x i d i z i n g w a t e r s at h i g h tide and less oxidizing, and e v e n reducing, w a t e r s at l o w tide, s e e m s to be the g e n e r a l pattern in m a n g r o v e waters. 51sO v a l u e s varied little during the c y c l e ( - 0.37 to - 0.74%0), being s l i g h t l y l o w e r t h a n t h e l o c a l s e a w a t e r v a l u e ( - 0.20%0) and m u c h h i g h e r t h a n t h e l o c a l f r e s h w a t e r v a l u e ( - 4.70%0) (Fig. 3). T h e r e s u l t s are a reflection o f t h e a b s e n c e o f s i g n i f i c a n t f r e s h w a t e r inputs to the creek, i m p l y i n g that t h e tides are the m a i n s o u r c e of material, i n c l u d i n g metals, to the area.

174

Characterization of suspended matter during the tidal cycle The concentration of SM flowing in and out of the mangrove forest through creek waters is shown in Fig. 5. Maximum SM concentration occurs during inversions of water fluxes at the beginning of high and low tides. During the peak of the low and high tides, constant, minimum values of SM were recorded. Again, this behaviour occurred in the two tidal cycles monitored. Table 1 shows 613C values for selected components of the mangrove ecosystem studied and of SM from different sources. The results show a consistent difference between the organic matter from marine and mangrove origin, making possible the differentiation of SM from the two sources. It is

m~.r [

~3--(3 rnql-I 13C/12C

~,

~80

0--0

DAY 26/02/86

140

~20D~.h lO0(ml

J -25.0

40

-23.0

~0 0.5

-21.0

n~.i-I DAY

25/02/86

~

~20 I00 (m)

13C/12C - 2"~0 -25.0 -23.0 -21.0

~ . . . . . . . . .

TABLE

0

~

~5

---

,', F i g . 5.

I.o

,'2

h

14

,'5

~

,6

,

C~

,'7

,'s

~

~0

80

2,0

60

1.5

40

LO

20

0.5

,'9 .(.)

Total suspended matter and 13C/~20 ratio of suspended matter during two tidal cycles.

1

values for different components of a mangrove ecosystem in Sepetiba Bay, Rio de Janeiro. The values are means or intervals of three samples, except for sediments, for which 12 samples were determined ~13C

Mangrove components

~:~C (%o, P D B )

mangle leaves Mangrove sediments Mangrove suspended matter B a y ' s suspended matter

- 27.6 -26.6 + 0.5

R.

- 25.5 t o - 2 6 . 8 - 20.5

175 also clear that mangrove leaves are the principal source of organic carbon to sediments and mangrove SM. In order to estimate the relative contributions of marine and terrestrial carbon sources during the tidal cycle, a simple "two end-members mixing model" was used using the 613C of - 21%o for the marine end-member and 613C of - 27%0 for the mangrove end-member, the R. mangle leaves value (Lacerda et al., 1986b). The variation of 613C values in SM and of the percent contribution of the two main sources are also shown in Fig. 5. Again, the general trend was similar for the two cycles monitored. At the peak of low tide, 513C values are lowest ( - 25.0%0), corresponding to a contribution from the mangrove source of between 60 and 70%. At the peak of high tide, 513C values are closest to that of the marine end-member ( - 21.3%o), corresponding to a contribution of the marine source varying from 90 to 100%. Therefore, during low tides, most of the organic carbon exported originates from mangrove plant detritus, while during high tides almost all of the organic carbon imported by the ecosystem is of marine origin.

Trace metal concentration in suspended matter during tidal cycles Concentrations of trace metals in SM during tidal cycles are presented in Fig. 6. Again, variations of metal concentrations were similar in the two cycles. Three different patterns of variation are clear. The first, represented by Fe, showed irregular and small variability in concentration throughout the cycle. The second, represented by Mn, showed a significant concentration peak during rising tide, coincident with the highest variation in pH and Eh (Fig. 4). Lowest Mn concentrations were measured during the peak of low tides, and intermediate values during peaks of high tide. The third pattern is represented by the variations in the concentrations of all other metals, including Cu, Cd, Pb, Ni, Cr and Zn, which showed significant concentration peaks during the peak of high tide. A smaller peak in the concentrations of these metals also occurred during rising tide, coincident with the Mn peak. During low tide periods, all these metals occurred in lower and relatively constant concentrations in SM. DISCUSSION It has been shown that there was a great variability in physico-chemical parameters during the tidal cycle, including changes in SM and metal concentrations. Some variability has been shown to occur in other coastal wetland ecosystems consisting of either salt marsh or mangrove (Nixon, 1980; Woodroffe, 1985c). However, significant differences between sources of SM during the tidal cycle have been poorly documented in the literature, and this proved to be important for the understanding of trace metal behaviour in the mangrove.

176 DAY 25/02/86 I00f 50 0

Cr O~

150t 90 50

(a)

o__ o/O--~oJ°~o-___

/ - - 0

O~

~

o

o

0

~ 0 0

ZOI 40 I0

0 - -

ICOI

Ni

Cd

O~

0--0~0~

6o i 20"

o/

0

I00 6O 20 800

,'°f o---~_

o -

.

/\

~o

°~o

0

o

o

- o ---~-._o/ ~ d

j\

;tOO

Iooo 8oo 6oo

o~o.f~°~

o~ o / ° - ~

zn

6oo

400

~0~__0

o ~

4OO

o

0 fO-,~

o

Depth (m)

0 ~ 0

2OO

:f

o

11

~

/o

b

o

20 1.5 1.0

05

2O 0

II

12

13

14

15

16

17

18

19

t(h)

Fig. 6. (a) Trace metal concentrations (#g g- 1DW) in suspended matter during the cycle monitored on 25 February 1986. (b) Trace metal concentrations (pg g 1DW) in suspended matter during the cycle monitored on 26 February 1986. Our results indicate a c o m p l e x i n t e r a c t i o n a m o n g the different parameters c o n t r o l l i n g metal fluxes t h r o u g h the system, and the effects depend upon the metal involved. The c h a n g e in SM source is the principal parameter involved. C h a n g e s in water pH and Eh, and m a n g a n e s e precipitation, can also a c c o u n t for a s e c o n d a r y peak in trace metal c o n c e n t r a t i o n s during the tidal cycle. The influence of the parameters measured on the b e h a v i o u r of Fe in SM however, is not clear, since Fe was present in higher concentrations, at least 3 or 4 orders of m a g n i t u d e greater, than the other elements in both m a n g r o v e and bay SM

177

(b)

DAY 2 6 / 0 2 / 8 6

80

o

Cr

60

0 --

--0 ~0/0 ~

0 -°~o/

o 2001 Cu IO0

o

o 6° 40f

Cd o_

Z.O

~°~o-O~o ° ~

120f 8O

o

~ o

~

o

Pb

/ ~°~o//°~o

4O

o~O~.~/° o~ o O ~ o / /

~ ° ~ _ _ o ~ o--o

0

o~ o - - o

0~

DePth (m)

0~ "

II

12

13

14

15

~~

16

17

18

i 1.5

19

(Lima et al., 1986), therefore small changes in Fe concentrations could not be detected. The behaviour of Mn, however, can be affected by the changes in pH and Eh (Krauskopf, 1979). During rising tide, an increase in the redox potential from 156 to 226 mV and of pH from 7.02 to 8.17 can occur, which would acount for the oxidation of Mn 2÷ to Mn 4+, resulting in precipitation of Mn on SM particles, probably as colloidal Mn oxy-hydroxide (Balikungeri et al., 1985). This process would probably be biologically mediated, accelerated by the high temperatures (25.~32.0°C) typical of the area (Vojak et al., 1985). Harbison (1986) reported this same behaviour of Mn in mangrove waters in Australia. The precipitation of Mn could scavenge other metals from solution and may be responsible for the small, secondary peak in the concentration of some metals in SM, in particular

178

Cu, Pb and Ni, and possibly even Fe. This role of Mn hydrous-oxides has been extensively reported as a main factor controlling metal distribution in natural waters (Salomons and FSrstner, 1984). The increase in concentration of all metals, with the exception of Fe and Mn, occurred during the peak of high tide, coincident with a shift in SM source to the creek water. During most of the cycle, SM is partially mixed (mangrove plus marine born SM), with a preponderance of mangrove-derived SM. At the peak of high tide, SM in the creek is almost totally of marine origin. Sepetiba Bay is contaminated with trace metals (Lacerda, 1983) and the bay's SM has been identified as the principal pathway of transport of metals through the bay (Lacerda et al., 1983, 1985; Lima et al., 1986). Therefore, the dominance of SM of marine origin at the peak of the tide would bring particles of high metal content to the mangrove, while mangrove particles with low metal content would characterize SM during the rest of the cycle. These results suggest that marine SM with elevated metallic load is being actively trapped by the mangrove environment, which would act as an efficient sink for metals. The immobilization mechanism might include the binding of settled SM by the tangled mat of small roots abundant in the mangrove sediment (Harbison, 1986). Once immobilized in sediments, rapid exchange of metals from marine SM to mangrove sediments would occur, in particular to organic matter (Lacerda and Abrfio, 1984) and HS , which fixes most metals as insoluble sulphides (Linderberg et al., 1982; Harbison, 1986). This latter process may be very rapid (Howarth, 1979) under the conditions found in mangrove sediments (Lacerda and Rezende, 1984). Our results, however, cannot fully explain the immobilization process involved. The possible net accumulation of metals in mangroves by the processes discussed above, will also depend on the quantities of SM entering and leaving the system. Our results show that there is a great difference in metal concentration between marine and mangrove SM. Only if the SM export is large in relation to the import would metals not accumulate in mangroves. Mass balance studies in mangrove areas are scarce, and no general pattern can yet be presented. Therefore, although our data strongly point to an accumulation hypothesis, mass balance studies have to be performed before a generalization can be made. ACKNOWLEDGEMENTS

This paper was supported by Financiadora de Estudos e Projetos (FINEP) and by Conselho Nacional de Desenvolvimento Cientifico e TecnolSgico (CNPq) of Brazil. Thanks are due to the Universidade Federal Rural do Rio de Janeiro for the use of field facilities. Part of this manuscript is a result of the fruitful discussion with colleagues from the Institute of Geology, and Paleontology of the University of Hamburg, in particular Dr V. Ittekott, through a GKSS (F.R.G.)-CIRM (Brazil), joint program (M-12) on Mangrove Biogeochemistry. The two institutions are gratefully acknowledged.

179 REFERENCES Adaime, R.R., 1985. Producao do bosque de mangue de Gamboa Nobrega (Cananeia, Brasil). T. Dout., Universidade de Sao Paulo, Instituto Oceanografico, Sao Paulo, 350pp. Balikungeri, A., D. Robin and W. Haerdi, 1985. Manganese in n a t u r a l waters. Evidence for microbiological oxidation of Mn(II). Toxicol. Environ. Chem., 9: 309-325. Banus, M.D., 1977. Copper, iron and manganese content of mangrove seedling from Puerto Rico. Proc. 15th Annu. Hanford Life Sci. Symp., Richland, Washington, pp. 380-389. Boto, K.J. and J.S. Bunt, 1981. Tidal export of particulate organic matter from a N o r t h e r n Australian mangrove system. Estuarine Coastal Shelf Sci., 13:247 255. DeLaune, R.D., C.N. Reddy and W.H. Pattrick Jr, 1981. Accumulation of plant nutrients and heavy metals through sedimentation process and accretion in a Louisiana salt marsh. Estuaries, 4: 328--334. Fiszman, M., W.C. Pfeiffer and L.D. Lacerda, 1984. Comparison of methods used for extraction and geochemical distribution of heavy metals in botton sediments from Sepetiba Bay, Rio de Janeiro. Environ. Technol. Lett., 5: 567-572. Gallagher, J.L. and H.V. Kibby, 1980. Marsh plants as vectors in trace metal transport in Oregon tidal marshes. Am. J. Bot., 67: 1069-1074. Giblin, A.E., A. Bourg, I. Valiela and J.M. Teal, 1980. Uptake and losses of heavy metals in sewage by a New England salt marsh. Am. J. Bot., 67: 1059~1068. Harbison, P., 1981. The case for the protection of mangrove swamps: geochemical considerations. Search, 12: 273-276. Harbison, P., 1986. Mangrove muds A sink and a source for trace metals. Mar. Pollut. Bull., 17: 246- 250. Heald, E.J., 1969. The production of organic detritus in a South Florida estuary. University of Miami Sea G r a n t Program, Miami, Florida. Howarth, R.W., 1979. Pyrite: Its rapid formation in a salt marsh and its importance in ecosystem metabolism. Science, 203: 49-50. Jouaneau, J.M., H. Etcherber and C. Latouche, 1983. Impoverishment and decrease of metallic elements associated with suspended matter in the Gironde estuary. In: Wong, Boyle, Bruland, Burton and Goldberg (Eds), Trace Metals in Sea Water. Plenum Press, New York. Krauskopf, K.B., 1979. Introduction to Geochemistry, 2nd edn. McGraw Hill Kogakusha, Tokyo. Lacerda, L.D., 1983. AplicaqSes de metodologia de abordagem pelos parfimetros critocos no estudo da polui~fio por metals pesados na Baia de Sepetiba, Rio de Janeiro. PhD Thesis, Inst. Bioflsica, Univ. Fed. Rio de Janeiro, 154 pp. Lacerda, L.D., 1984. Manguezais: Florestas de Beira Mar. Cienc. Hoje, 13: 62-70. Lacerda, L.D. and J.J. Abrfio, 1984. Heavy metal accumulation by mangrove and salt marsh intertidal sediments. Rev. Bras. Biol., 7: 49-52. Lacerda, L.D. and C.E. Rezende, 1984. Dinhmica de metals pesados em manguezais. In: II Simpdsio Brasileiro Sobre Recursos do Mar (in press). Lacerda, L.D.W.C. Pfeiffer and M. Fiszman, 1979. O papel de Paspalum vaginatum na disponibilidade de cromo para as cadeias alimentares estuarinas. Rev. Bras. Biol., 39: 985-989. Lacerda, L.D., W.C. Pfeiffer and M. Fiszman, 1983. Monitoring of heavy metal pollution through the critical pathways approach: A case study in Baia de Septetiba, Brazil. Proc. Int. Conf. Heavy Metals in the Environ., Heidelberg. CEP Consultants Ltd., Edinburgh, pp. 125t~1261. Lacerda. L.D., C.E. Rezende, D.M.V. Jos~, J.C. Wasserman, M.C.F. Francisco and J.C. Martins, 1985. A note on the mineral concentrations in leaves of mangrove trees. Biotropica, 17: 260-262. Lacerda, L.D., C.E. Rezende, D.M.V. Jos~ and M.C.F. Francisco, 1986a. Metallic composition of mangrove leaves from Southeastern Brazil. Rev. Bras. Biol., 46: 395-399. Lacerda, L.D., C.E. Rezende, L.A. Martinelli, A.R. Ovalle, A.A. Mozeto, F.B. Nogueira, R.F. Vitoria, G.T. Aragon, C.R. C u n h a and C.A.R. Silva, 1986b. Composiqfio issotSpica de carbano em componentes de um manguezal na Baia de Sepetiba, RJ. Cienc. Cult., 38:1714 1717. Lima, N.R.W., L.D. Lacerda, W.C. Pfeiffer and M. Fiszman, 1986. Temporal and spatial variability

180 studies of Zn, Cr, Cd and Fe concentrations in oyster tissues (Crassostrea brasiliana Lamarck, 1919) from Sepetiba Bay, Brazil. Environ. Technol. Lett., 7: 453~60. Lindberg, S.E., R.C. Harris and R.R. Turner, 1982. Atmospheric deposition of metals to forest vegetation. Science, 215: 160~1611. Nixon, S.W., 1980. Between coastal marshes and coastal waters - A review of twenty years of speculation and research on the role of salt marshes in estuarine productivity and water chemistry. In: P. Hamilton and K.B. MacDonald (Eds), Estuarine and Wetland Processes, Plenum Press, New York, pp. 437 525. Odum, W.E., 1984. Dual-gradient concept of detritus transport and processing in estuaries. Bull. Mar. Sci., 35: 51(~521. Pfeiffer, W.C., L.D. Lacerda, M. Fiszman and N.W.R. Lima, 1985. Metais pesados no pescado da Bala de Sepetiba, RJ. Cienc. Cult., 37:297 302. Salomons, W. and U. FSrstner, 1984. Metals in the Hydrocycle. Spring-Verlag, Berlin, 349 pp. Vojak, P.W.L., C. Edwards and M.V. Jones, 1985. Evidence for microbiological manganese oxidation in the River Tamar estuary, south-west England. Estuarine Coastal Shelf Sci., 20: 661-671. Woodroffe, C.D., 1985a. Studies of a mangrove basin, Tuff Crater, New Zealand: 1. Mangrove biomass and production of detritus. Estuarine Coastal Shelf Sci., 20: 265-280. Woodroffe, C.D., 1985b. Studies of a mangrove basin, Tuff Crater, New Zealand: II. Comparison of volumetric and velocity area method of estimating tidal flux. Estuarine Coastal Shelf Sci., 20: 431-445. Woodroffe, C.D., 1985c. Studies of a mangrove basin, Tuff Crater, New Zealand: III. The flux of organic and inorganic particulate matter. Estuarine Coastal Shelf Sci., 20: 447-461.