Anais da Academia Brasileira de Ciências (2011) 83(2): 391-407
(Annals of the Brazilian Academy of Sciences)
Printed version ISSN 0001-3765 / Online version ISSN 1678-2690
www.scielo.br/aabc
Biogeochemical processes and the diversity of Nhecolândia lakes, Brazil
TEODORO I.R. ALMEIDA1 , MARIA DO CARMO CALIJURI2 , PATRÍCIA B. FALCO2 ,
SIMONE P. CASALI2 , ELENA KUPRIYANOVA3 , ANTONIO C. PARANHOS FILHO4 ,
JOEL B. SIGOLO1 and REGINALDO A. BERTOLO1
1 Instituto de Geociências, Universidade de São Paulo, Rua do Lago, 562, 05508-080 São Paulo, SP, Brasil
2 Escola de Engenharia de São Carlos, Universidade de São Paulo,
Avenida Trabalhador Sãocarlense, 400, 13566-590 São Carlos, SP, Brasil
3 Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow, 127276, Russia
4 Centro de Ciências Exatas e Tecnologia, Universidade Federal do Mato Grosso do Sul, Cidade Universitária,
Avenida Costa e Silva, 1524, 79000-060 Campo Grande, MS, Brasil
Manuscript received on February 17, 2010; accepted for publication on October 5, 2010
ABSTRACT
The Pantanal of Nhecolândia, the world’s largest and most diversified field of tropical lakes, comprises approximately
10,000 lakes, which cover an area of 24,000 km2 and vary greatly in salinity, pH, alkalinity, colour, physiography
and biological activity. The hyposaline lakes have variable pHs, low alkalinity, macrophytes and low phytoplankton
densities. The saline lakes have pHs above 9 or 10, high alkalinity, a high density of phytoplankton and sand beaches.
The cause of the diversity of these lakes has been an open question, which we have addressed in our research. Here
we propose a hybrid process, both geochemical and biological, as the main cause, including (1) a climate with an
important water deficit and poverty in Ca2+ in both superficial and phreatic waters; and (2) an elevation of pH during
cyanobacteria blooms. These two aspects destabilise the general tendency of Earth’s surface waters towards a neutral
pH. This imbalance results in an increase in the pH and dissolution of previously precipitated amorphous silica and
quartzose sand. During extreme droughts, amorphous silica precipitates in the inter-granular spaces of the lake bottom
sediment, increasing the isolation of the lake from the phreatic level. This paper discusses this biogeochemical problem
in the light of physicochemical, chemical, altimetric and phytoplankton data.
Key words: Pantanal, alkaline lakes, saline lakes, cyanobacteria, alkalinization processes.
INTRODUCTION
The Pantanal is the largest floodable surface on Earth,
covering approximately 200,000 km2 (Fig. 1). It is located in the Pantanal Basin (Almeida 1945), an inland
tectonic depression that originated from tectonic interactions between the South American and Nazca Plates
during the Late Tertiary (Assumpção 1998, Ussami et
al. 1999). This basin has been filled by several alluvial fans, generating quaternary sediments dominated by
quartzose sands, with maximum thickness of approximately 550 m (Assine 2004). The Pantanal is divided
Correspondence to: Teodoro Isnard Ribeiro de Almeida
E-mail: talmeida@usp.br
into 11 sub-areas based on characteristics of seasonal
floods, physiography and ecology (Silva et al. 1998).
Two of these areas, Paiaguás and Nhecolândia, occupy
almost the entire alluvial fan of the Taquari River, with
an area of 54,125 km2 . This fan is a complex depositional system with an almost circular form approximately 250 km in diameter, the largest on the planet
(Assine 2004).
Nhecolândia, whose 24,000 km2 area occupies the
southern half of the Taquari alluvial fan (Fig. 1), has
200 m of altitude in the eastern most part and 80 m
near the Paraguay River. This alluvial fan is still active
with summer floods. The local annual rainfall is around
An Acad Bras Cienc (2011) 83 (2)
392
TEODORO I.R. ALMEIDA et al.
Fig. 1 – Localisation of Pantanal and the studied area (modified from Galvão et al. 2003).
1100 mm, lower than the annual evapo-transpiration rate
of 1400 mm (Por 1995). Lower Nhecolândia, which is
the study area, corresponds to the oldest depositional
lobe of the Taquari alluvial fan (Assine 2004). It is distinguished from other sub-areas of the Pantanal by its
uncommon physiography. This is characterised by the
presence of seasonally flooded savannas limited by forest fragments growing over elevations 1-3 m in height
(known locally as cordilheiras) and thousands of lakes
with high spatial, physical, chemical and biological variability. These lakes are shallow, and are usually classified according to their pH and electric conductivity (EC;
Almeida et al. 2003), pH and salinity (Costa and Telmer
2007), size, degree of roundedness and orientation (E.
Fernandes, unpublished data).
The saline lakes, locally named salinas, have
brackish-to-saline waters and basic pH (often above
10), are rarely deeper than 1 m, with an average depth
of approximately 50 cm in the rainy season (Galvão
et al. 2003), and rarely become dry. They are distinguished by beaches devoid of vegetation ringed by
a fringe of carandas palm trees (Copernicia alba MoAn Acad Bras Cienc (2011) 83 (2)
rang) and Gramineae, which in turn is surrounded by
carandas and Bromeliaceae popularly known as “caraguatá” (Aechmea spp.) and finally by the forest that
covers the cordilheiras. These elevations completely
surrounding the salinas protect them from the inflow
of water during the floods.
The hyposaline lakes, locally named baías, are
always devoid of beaches, have variable pH and low
to-very-low salinity and can surpass 2 m in depth (Furquim et al. 2010), although most lakes are around 1 m
in depth (Galvão et al. 2003). Aquatic vegetation is
common. While surrounded by cordilheiras, the protection of the inflow of waters can be only partial. Carandas are absent from these cordilheiras, which have another species of palm tree of equal importance, popularly known as bocaiúva (Acrocomia aculeata Lodd),
which are absent from the cordilheiras that surround
the salinas (Almeida et al. 2003). Also notable are
the relative altitudes of the saline and hyposaline lakes:
Almeida et al. (2009), using precision equipment, measured the altitude of the 55 lakes studied, finding lower
altitudes for the saline ones, and interpreted this as an
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
evidence of geochemical erosion of sediments through
quartz dissolution and reprecipitation of SiO2 as amorphous silica in the inter-granular spaces. This process
occurs only in saline lakes, resulting in their location
consistently below their hyposaline neighbours. The
depth of the baías increases from the margins to the
centre, unlike the salinas, which have flat sub-horizontal
bottoms. This was interpreted by Almeida et al. (2009)
as related to the interaction between the alkaline, silicarich solutions and the weakly acidic water table.
The pH variation is very important, ranging from
slightly acid to very basic (Almeida et al. 2003, Costa
and Telmer 2007). The salinity also varies strongly,
with values of up to 286 times in lakes in relatively
restricted geographical areas, according to Costa and
Telmer (2007). Considering the sodium content as
an indicator of salinity, the maximum difference was
27,145-fold (Barbiero et al. 2008). Such differences
are essentially due to the greater isolation of the salinas from phreatic recharge by continuous horizons of
greenish and grizzly soil of low porosity (Barbiero et
al. 2008). Despite these different salinities, Barbiero
et al. (2002) and Furquim et al. (2010) concluded that
the salinas and baías waters belong to the same chemical family, excluding the possibility that the salinity
is a legacy of past climatic periods. The isolation of
the saline lakes is associated with high alkalinity, which
helps to attack the quartzose sand and silt, supplying
2−
silica (in solution probably as H3 SiO−
4 or H2 SiO4 ) to
precipitate Mg silicates (saponite and stevensite), illite
and the amorphous silica cementing the grains of quartzose sand. This has been well described by Barbiero et
al. (2008) and Furquim et al. (2008).
The lakes of Nhecolândia have some similarity to
the soda lakes of the East African Rift Valley, considering the descriptions of Melack and Kilham (1974),
Duckworth et al. (1996) and Jones et al. (1998). Like
the Rift Valley lakes, the lakes of Nhecolândia have a
water deficit (Por 1995, Barbiero et al. 2008). The waters are poor in Ca2+ and Mg2+ (Barbiero et al. 2002,
Furquim et al. 2010), and there are frequent cyanobacteria blooms and an increase in salinity during the dry
season (De-Lamonica-Freire and Heckman, 1996, Oliveira and Calheiros, 2000, Medina-Júnior and Rietzeler
2005). It is important to note that the hypothesis that
393
alkalinisation in the lakes of Nhecolândia originates
from carbonate massifs has been completely discarded.
A biogeochemical origin, as in the Rift Valley lakes, is
the only remaining possible explanation.
De-Lamonica-Freire and Heckman (1996) described 337 planktonic species in the northern part of
the Pantanal, verifying a dominance of cyanobacterial
species in the dry season and their absence during
floods. Because the region is subjected to an intensely
dry period between May and October, these authors
suggested that the high proliferation of cyanobacteria
is associated with increases in salinity, but did not
show a relation between the bloom of these organisms
and pH, although there was a positive correlation with
salinity, as is normal in alkaline lakes. In their quantitative study of the plankton species of the Paraguay
River and its flood plains, Oliveira and Calheiros (2000)
identified 82 species. Similar to De-Lamonica-Freire
and Heckman (1996), these authors found that Chlorophyceae were prevalent and Cyanobacteriae were present only in the dry season. These studies confirm the
general rule of nature, that the more severe the environmental conditions, the lower the biodiversity and the
denser the population of surviving organisms (Sergeev
et al. 2002) This explains the prevalence of cyanobacterial extremophiles in the saline waters of Nhecolândia,
as observed in all prior studies (Oliveira and Calheiros
2000, Santos et al. 2004, Medina-Júnior and Rietzeler
2005, G. Mourão, unpublished data). The high evaporation rate during the dry season and the simultaneous
biochemical processes (mainly the absorption of CO2
by phytoplanktonic productivity) increase the salinity
and alkalinity to adverse levels for most phytoplanktonic species. Since the prevalence of any species in
an environment depends on its superior survival ability (Tilman 1977), only the more resistant species will
survive in high salinities and pHs. Cyanobacteria tend
to occupy more ecologically adverse niches (Esteves
1998), and thereby have a higher survival ability. This
explains why they were probably the first organisms to
appear on Earth, as evidenced by fossils in rocks of 3.5
to 3.8 Ga (Westall 2005). The high proliferation level of
cyanobacteria is explained by the absence of competitors; their resistance to high salinity, high temperatures
and low oxygen levels (Silva et al. 2008); their freedom
An Acad Bras Cienc (2011) 83 (2)
394
TEODORO I.R. ALMEIDA et al.
from zooplankton predation; their accessory pigments
such as phycobilins, which increase their capacity to absorb solar electromagnetic radiation in the green wavelength; and their ability to control their buoyancy and
thereby migrate through the water column to enhance
their photosynthetic activity (Shapiro 1990). It has been
observed that shallow lakes favour the development of
dense phytoplanktonic populations and that the salinas
are shallower than the baías (Galvão et al. 2003). It is
evident that in Nhecolândia there is a correlation between pH and salinity (Almeida et al. 2003, Galvão et
al. 2003, Costa and Telmer 2007). This indicates that
the alkalinisation and salinisation processes are interdependent. A correlation between salinity and phytoplanktonic activity has been described, but the possibility of cause and effect relationships among the alkalinity, salinity and phytoplanktonic activities has not
been discussed in the literature.
The available data indicate that the Nhecolândia
physiography arises from the complex and only partially understood combination of biological, hydrological,
climatic, sedimentary, geochemical and neotectonic processes. To explain the diversity of lakes, however, we
propose a hybrid process based on the phytoplankton
activity and hydrogeochemistry of the saline and hyposaline lakes.
ALKALINE LAKES AND THE BIOGEOCHEMICAL
PROCESSES INVOLVED
The geochemistry of calcium and its carbonates has a
fundamental role in the preservation of the pH balance
in waters: pH is increased through the dissolution of
2−
carbonates (releasing HCO2−
3 and CO3 species into the
water) and reduced through the precipitation of CaCO3
(removing CO2−
3 from water). Hence, the condition of
neutral pH, that is conducive for most terrestrial organisms, is attained in the presence of calcium, which
stabilises the pH between 5.5 and 8.5 (Zavarzin 2002).
According to this author, three routes of calcium capture can be considered: (1) abiotic chemical precipitation of carbonates of calcium, caused by physical and
chemical imbalance in the water, such as the saturation
of the solution because of evaporation; (2) a biological
route where the carbonate precipitation is caused by
the alkaline barrier created by the activity of microorAn Acad Bras Cienc (2011) 83 (2)
ganisms; and (3) direct precipitation in the construction
of skeletons by intracellular mineralisation. The dissolution of the carbonates is caused by reverse processes:
an increase in CO2 concentration by respiration in the
oxygenated zone, or by the anaerobic generation of
organic acids.
Soda lakes constitute the most natural alkaline environment on the planet, with pHs as high as 12. The formation of such lakes requires low Ca2+ and high Na2+
contents, tropical arid or semi-arid zones with a water
deficit, and salinisation through evaporation. The increase in the alkalinity is due to the disequilibrium in
2−
2−
the CO2 / HCO−
3 / CO3 system to CO3 arising from
the impossibility of precipitating CaCO3 (Duckworth
et al. 1996). The persistence of alkaline lakes, however, requires a continuous process of alkalinisation to
annul the buffering effect of CO2 (Jones et al. 1998).
In agreement with McConnaughey and Whelan (1997),
the most elementary mechanism of photosynthetic alkalinisation of water results from the liquid capture of
−
CO2 , leading to the concentration of CO2−
3 and OH .
If the water is oversaturated with CaCO3 , precipitation
is induced biogeochemically, with a resulting drop in
pH to near neutrality and an enrichment of Na+ and
Cl− in the solution. By contrast, high primary photosynthetic productivity, mainly due to a dense cyanobacterial population during blooms, will bring a decrease
in the dissolved HCO−
3 and thereby a biogenic enrichment in CO2−
.
With
a
deficiency in Ca2+ to precipitate
3
CaCO3 , the pH necessarily rises (Visscher et al. 1998).
Thompson and Ferris (1990), using cultures of Synechococcus, a cyanobacterium, demonstrated the pericellular precipitation of gypsum, calcite and magnesite
parallel to an increase of the pH from 7.97 to 8.57 in
72 hours. This is a fast rate of alkalinisation, although
in the experiment there were Ca2+ and Mg2+ present to
minimise the pH increase.
Until recently, the enzyme carbonic anhydrase (CA)
was known as an enzyme that catalyses the reversible
+
hydration of CO2 (CO2 + H2 O ⇆ HCO−
3 + H ) in
many eukaryotes. Close to the end of the 1990s it was
discovered to be much more common and omnipresent
in the domains of Archaea and Bacteria (Smith et al.
1999). Some eukaryotic algae can precipitate intracellular CaCO3 through the activity of CA. However, the
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
cyanobacteria promote this activity only pericellularly.
The internal pH of these organisms is neutral – their
CA promotes external alkalinisation by OH− excretion,
whereas fixing CO2 from HCO−
3 generates pericellular CaCO3 precipitation (Kupriyanova et al. 2007). In
other words, cyanobacteria promote the intense capture
of inorganic carbon in the form of CO2 or HCO−
3 not
only by photosynthetic activity during blooms (similar
to other microorganisms), but also by the extra cellular activity of CA, which alkalinises their environment.
For this reason, these organisms are particularly efficient in raising the pH of the water. According to Kupriyanova et al. (2007), the intensity of cyanobacterial CA
activity is strictly controlled by pH, with a maximum at
pH 9.8, which is the ideal pH for these organisms. Thus,
at pH > 9.8 the CA probably becomes increasingly less
effective at raising alkalinity.
MATERIALS AND METHODS
Lakes were chosen for sampling using remote sensing
images whose spectra were influenced by the phytoplankton content (Galvão et al. 2003). Real-colour TMLandsat 5 and AVNIR2-ALOS images were employed.
Three field campaigns were conducted to collect
water samples in different seasons. Initially, these studies were planned for the same group of lakes at the Rio
Negro farm, but only one set of water samples could
be collected there, so the other two sets were acquired
from the neighbouring Barranco Alto farm. The first set
of samples was collected from 18 to 25 August 2007, in
the middle of a rigorous drought. The second collection
period was from 10 to 19 July 2008, at the beginning
of drought, as the rainy season had extended into June.
The third was from 6 to 10 October 2008, at the end of
the normal dry season, but in a less intense drought than
that of August 2007.
The three different groups of data are independent,
considering the dynamics of the environment. At the
same time, it was possible to compare a sub-set of samples, collected at two different climatic situations, from
the same group of lakes. Finally, although the ensemble
had problems (being sampled over two years), it is possible to consider three sets of samples: those taken at the
beginning (July 2008), the middle (October 2008) and
the end of the dry season (August 2007).
395
The temperature of the water (◦ C), the EC
(µS.cm−1 ), the dissolved oxygen (% and mg.L−1 ) and
the pH were measured in situ with a multi-probe instrument (Yellow Springer, 556 MPS). Samples of water
were collected close to the centre of the lakes in polyethylene flasks, filtered with Millex filters with a 0.45
membrane and then frozen. The samples of the first
campaign were taken to the Laboratory of Groundwater Research Centre at the Institute of Geosciences of
São Paulo University (USP) for cations analysis. Na+
and K+ were analysed by flame photometry, and the
other cations by atomic absorption spectrophotometry.
The samples from the two other collection sets were sent
to Activation Laboratories (Toronto, Canada) for similar cation analysis by ICP-OES or ICP-MS, according
to the salinity identified in the field by EC. The anions
were analysed by ion chromatography in the laboratories of the Engineering School of São Carlos (USP).
For the determination of phytoplankton, the water
samples were collected and fixed with an acetic Lugol
solution. The phytoplankton was counted using the sedimentation method (Uthermohl 1958). From the quantitative analysis, the total density (organisms.mL−1 ) was
calculated according to the equation below (APHA
1995):
C × At
D(org/mL) =
Af × F × V
where
D = total density (organisms.mL−1 );
C = number of organisms counted;
At = total surface area of the sedimentary bed (mm2 );
A f = surface area of the field of counting (mm2 );
F = number of counted fields;
V = volume of the sediment (mL).
The relative abundance was estimated considering
the number of individuals of each species and the total
number of individuals, according to the classification of
McCullough and Jackson (1985): 50 to 100%, dominant organisms; 30 to 49%, abundant organisms; 10 to
29%, common organisms; 1 to 9%, occasional organisms; <1%, rare organisms.
To determine the concentrations of chlorophyll a
and pheophytin, the samples were filtered through glass
microfibre membranes (Millipore AP 20; 47 mm diameter and 8.0 µm porosity), and stored frozen until the
An Acad Bras Cienc (2011) 83 (2)
396
TEODORO I.R. ALMEIDA et al.
TABLE I
Classification by EC (µS.cm−1 ) adopted for the lake waters studied
and the approximate content of total dissolved solids (TDS)
calculated by the mean value reported in APHA (1995).
Classes of waters
Freshwater
Water with low or average salinity
Water with high salinity
Water with very high salinity
Hypersaline water
moment of extraction. Ethanol at 80% was used for the
extraction. The spectrophotometric analysis of the extracts was performed according to APHA (1995), and
the reading was done between wavelengths of 665 and
750 nm. For the determination of chlorophyll a (µgL−1 )
and pheophytin (µg.L−1 ), the following formulas were
used as in Nush (1980):
Chlorophyll a = 29.6
× {(Eu 665 − Eu 750 ) − (Ea665 − Ea750 )}
(1)
× v/V × s
Pheophytin = 29.6
× {[1.7 × (Ea 665 − Ea 750 )] − (Eu 665 − Eu 750 )} (2)
× v/V × s
where:
Eu = absorbance of the unacidified sample;
Ea = absorbance of the acidified sample;
v = volume of the bed (mL);
V = volume of the filtered sample (L);
s = thickness of the cuvette (cm);
29.6 = specific absorption coefficient of chlorophyll a;
1.7 = ratio of the yield of unacidified to acidified chlorophyll a.
The quantitative and qualitative analyses of the phytoplankton and chlorophyll concentrations were done in
the Laboratory of Biotoxicology of Continental Waters,
of the USP School of Engineering, São Carlos campus.
The Rio Negro farm samples were given the general acronym RN, added to the lake code according to
the sampling order, and the letter “s” for salinas or “b”
for baías. Samples from the Barranco Alto farm have
only the BA acronym followed by the lake number. All
An Acad Bras Cienc (2011) 83 (2)
EC
(µS.cm−1 )
< 100
100 to 750
750 to 2250
2250 to 5000
> 5000
Approximated
TDS (g.L−1 )
< 0.06
0.06 to 0.5
0.5 to 1.4
1.4 to 3.1
> 3.1
water samples were classified by their EC proportional
to the salinity according to Table I, modified from the
classification by USSL (1954).
RESULTS AND DISCUSSION
In August 2007 at the Rio Negro farm, water from 15
lakes was sampled for limnological and hydrogeochemical analyses. Eight of these lakes were salinas (EC >
750 µS.cm−1 ). In July 2008, 28 lakes were sampled, of
which 14 were salinas. In October 2008, 19 lakes were
sampled for hydrogeochemistry and 14 for limnological analyses, of which seven were EC < 750 µS.cm−1
and 12 EC > 2,000 µS.cm−1 . The results of the chemical analyses showed that all the waters were extremely
poor in Ca2+ and Mg2+ but, in the salinas, rich in Na+
and K+ , as stated in the general literature (Zavarzin
2002) and that on Nhecolândia (Barbiero et al. 2002,
Furquim et al. 2008). Table II presents the results of the
August 2007 sampling, where the poverty in Ca2+ and
Mg2+ ions is clear. The independence of these cations
with regard to EC and pH is evident. The Na and K
cations have a high correlation with EC, as expected,
it being almost perfect in the case of Na+ if we ignore
sample RN7S (R2 = 0.9997).
The fieldwork at the Barranco Alto estate, in July
and October 2008 yielded similar results (Table III).
For most of the water samples with a high pH, the content of dissolved calcium was below the detection limit,
as expected, because, in these conditions, Ca2+ precipitates as CaCO3 . It is important to observe that the high
Na+ and K+ content occurred only in the saline lakes because of evaporation from the lakes, which are isolated
from phreatic recharge. As regards the phytoplanktonic
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
397
TABLE II
EC, pH and content in mg.L−1 of Ca2+ , Mg2+ , Na+ and K+
of samples from the Rio Negro farm lakes (August 2007).
Lake
EC
µS.cm−1
pH
Ca
Mg
mg.L−1
Na
K
RN1B
RN1S
RN2B
RN2S
RN3B
RN3S
RN4S
RN5B
RN5S
RN6B
RN6S
RN7B
RN7S
30
2858
74
3467
110
2429
2798
591
7156
42
11500
27
8572
8.11
9.41
8.52
9.06
7.13
9.7
9.37
7.32
9.4
8.28
9.41
7.33
9.51
2.8
3.7
5.1
6.6
4.6
4.7
4.1
4.2
2.9
1.8
11.0
0.98
4.5
2.0
0.14
4.5
4.1
4.8
0.15
3.1
8.1
0.26
2.0
0.91
1.1
1.0
8.3
906
12.3
1060
23.1
762
813
152
2222
4.7
3600
7.5
1353
6.7
340
9.5
245
17.2
293
155
36.1
478
9.4
805
4.9
280
material, 28 lakes (salinas and baías) were sampled in
the first round and 19 in the second.
Table IV shows the percentages of lakes in relation
to the classes of the prevalent phytoplanktonic organisms in each of the five classes of water as described in
Table I. The 61 samples, as well as each contemporaneous set, confirm the conclusion of Oliveira and Calheiros (2000), Santos et al. (2004), Oduor and Schagerl
(2007) and Santos and Sant’Anna (2010) that cyanobacteria are more prevalent in more saline waters. When
the results from the same groups of lakes sampled in
July and October 2008 are compared, the seasonal variations replicate the findings of other authors. The sampling of August 2007 does not represent a climatically
intermediate situation, as indicated by the salinity and
stable isotope data, possibly reflecting climatic differences between 2007 and 2008. Two readings could be
made from Table IV: the seasonal evolution and, for
each sample collection, the distribution of classes of
organisms as a function of salinity. For the July 2008
collection, a continuous increase in the proportion of
cyanobacteria was observed in relation to the salinity.
For the August 2007 sample collection, the distribution
was irregular, though with a clear tendency towards the
growing dominance of cyanobacteria in the high-salinity lakes. However, this does not give an intermediary
view between the sample collections of July and October 2008. These data show the difficulty in comparing,
for detailed observations, different lakes and sample collections from different years. We were surprised to find,
among the high salinity lakes, with EC>5000µS.cm−1 ,
a lake with a predominance of Bacillariophyceae rather
than Cyanobacteriae. Finally, for the October 2008 collection, normally the most adverse situation because it
would be at the end of the dry season, cyanobacteria
were prevalent even in lakes with low-to-medium salinity. However, Chlorophyceae were dominant in a lake
of high salinity. The seasonal tendency is clear for the
sample collections taken from the same lakes; namely,
there is an increase of cyanobacterial dominance during the dry season. In relation to the salinity, the water
classes have the same tendency, with the prevalence of
cyanobacteria in the most saline waters. Considering
the number of genera and species (Table V), the tendency for the increase of cyanobacteria is continuous from
the freshwater to very saline waters. However, there is
an unexpectedly reduced presence of cyanobacteria in
the hypersaline water class.
The diversity of phytoplankton and the proportion
of cyanobacteria in relation to all phytoplankton organisms are, in general, highly correlated to water classes
from Table I (Tables VI and VII). The low number of
An Acad Bras Cienc (2011) 83 (2)
398
TEODORO I.R. ALMEIDA et al.
TABLE III
EC, pH and content in mg/L of Ca2+ , Mg2+ , Na+ and K+ of samples from the Barranco Alto farm lakes
in July and October 2008.
Lake
EC
uS/cm
First sampling (July 2008)
Ca
Mg
Na
pH
mg/L mg/L mg/L
BA01
BA02
BA03
BA04
BA05
BA07
BA08
BA09
BA12A
BA12B
BA14
BA16
BA21
BA22
BA23
BA24
BA25
BA26
BA27
BA30
BA31
BA32
BA33
BA34
BA35
BA36
BA37
BA40
25
113
172
77
3185
2932
27
4140
1045
1160
2517
3618
7188
5357
40
1590.5
710
2671
10
81
95
154
438
1001
780
940
1750
36
6.02
7.09
7.77
4.88
9.3
9.31
5.89
9.44
8.71
8.98
9.49
9.46
9.33
9.25
6.74
9.38
9.28
9.5
6.5
7.69
6.5
7.74
9.52
9
9.09
8.89
9.28
7.89
1.4
4.3
4.6
2.5
< 0.6
< 0.6
0.7
< 0.6
< 0.6
7.4
< 0.6
12
15
< 0.6
2.8
13
< 0.6
12
0.6
5.9
2.1
5.5
1.9
2.9
< 0.6
3.7
< 0.6
1.8
0.8
2.3
2.6
0.6
0.29
0.99
0.4
5.56
0.74
2.15
0.45
1.16
1.97
1.69
0.8
1.75
0.41
1.41
0.4
2.3
1.08
3.2
0.2
0.26
1.23
1.42
0.28
0.911
2.1
12.4
22.3
22.8
744
803
5.2
837
14.6
0.448
542
1320
2730
1770
9.6
527
260
980
2.8
16.2
18.2
35.9
356
0.321
229
0.316
600
2.5
genera and species in the freshwater lakes could be
because more complete limnological data were taken
from only one freshwater lake, thereby artificially reducing the diversity. For the other classes, the pattern
of diversity reduction with salinity increase is clear,
above all when all data are considered. It is clear that
this cyanobacteria association is more prevalent in
more saline waters, except for the hypersaline class
(Table VI and VII). In the latter, only cyanobacteria
were expected, because they are extremophiles organisms, thus more adaptable at a hypersaline environAn Acad Bras Cienc (2011) 83 (2)
K
mg/L
EC
uS/cm
3.6
13.6
17.9
5.4
128
178
3
148
3.9
98.2
166
359
324
207
5
139
103
227
2.8
19
34
29.5
110
158
196
111
127
6.26
36
161
229
–
4567
5641
–
6607
–
–
–
8410
16360
12870
79
3976
2317
6857
67
225
170
–
–
–
2032
2116
3940
–
Second sampling (October 2008)
Ca
Mg
Na
pH
mg/L mg/L mg/L
7.89
8.35
8.77
–
9.21
9.6
–
9.67
–
–
–
9.77
9.78
9.67
5.69
10.06
9.68
9.85
6.9
6.35
8.69
–
–
–
9.45
9.19
7.98
–
1.7
4.6
6.3
–
< 0.6
< 0.6
–
< 0.6
–
–
–
13
22
< 0.6
3.4
11
< 0.6
25
2.5
2.2
6.8
–
–
–
< 0.6
< 0.6
< 0.6
–
0.848
1.62
1.95
–
0.57
1.21
–
3.19
–
–
–
2.87
4.05
1.57
0.956
2.8
0.71
3.85
0.98
0.867
2.73
–
–
–
1
0.84
0.47
–
1.53
22
40.1
–
871
1130
–
1330
–
–
–
1680
3340
2410
13.7
843
332
1540
5.72
15.8
14.5
–
–
–
199
320
791
–
K
mg/L
4.27
17.5
19.8
–
148
250
–
198
–
–
–
430
799
597
6.63
159
141
342
5.37
37.7
20.2
–
–
–
191
128
173
–
ment. However, they have a lesser presence than in the
highly saline class lakes, yielding more space for Chlorophyceae and Cryptophyceae (Table V). If this situation was observed in only one field campaign, it might
be considered an exception. Because it was seen in all
three field campaigns, it suggests an unexpected and
unexplained trend. Table VII shows that, for the other
salinity groups, there is a distinct increase in cyanobacterial dominance from the beginning to the end of
the dry season except in the hypersaline waters, where
their dominance remained the same.
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
399
TABLE IV
Distribution of the percentage of classes of prevalent phytoplankton organisms in relation to the
total number of phytoplanktonic classes described for the groups of lakes classified according
to Table I. Cyanobacteria = Cyano; Chlorophyceae = Chloro; Bacillariophyceae = Bacill;
Cryptophyceae = Crypto; Dinophyceae = Dinophy.
Class of water
Freshwater (July 2008) n = 7
Freshwater (August 2007) n = 4
Freshwater (October 2008) n = 1
Average for freshwater
Low to average salinity (July 2008) n = 5
Low to average salinity (August 2007) n = 3
Low to average salinity (October 2008) n = 4
Average of low to average salinity
High salinity (July 2008) n = 8
High salinity (August 2007) n = 0
High salinity (October 2008) n = 4
Average of high salinity
Very high salinity (July 2008) n = 6
Very high salinity (August 2007) n = 4
Very high salinity (October 2008) n = 4
Average of very high salinity
Hypersaline (July 2008) n = 2
Hypersaline (August 2007) n = 4
Hypersaline (October 2008) n = 1
Average of hypersaline
Analysis of the density of organisms in the two
sample collections from the Barranco Alto farm with the
EC and pH data (Table VIII) demonstrated two different behaviours. The freshwater lakes with the phreatic
recharge had a small increase in salinity with increased
pH, essentially because of the activity of microorganisms. The lakes with saline water had a pH increase related to more intense activity of microorganisms, including blooms, but with a large increase in salinity because
of evaporation. The greatest geochemical imbalance was
caused by intense evaporation over lakes that are necessarily isolated from the water table. It was observed that:
(1) in the sample collections at the end of the dry season, three lakes showed cell densities > 106 ;
(2) these lakes have higher pHs;
(3) the lakes with higher EC had a low density of organisms at the beginning of the dry season and the
greatest density at the end of dry season;
Class of prevalent organisms (% of lakes)
Cyano Chloro Bacill Crypto Dinophy
25
25
0
50
0
50
25
0
0
25
25
75
0
0
0
33.3
41.7
0.0
16.7
8.3
66
33
0
0
0
0
33
0
66
0
100
0
0
0
0
55.3
22.0
0.0
22.0
0.0
75
25
0
0
0
*
*
*
*
*
87.5
12.5
0
0
0
79.2
18.8
0.0
0.0
0.0
80
20
0
0
0
50
25
25
0
100
0
0
0
0
76.7
15.0
8.3
0.0
0.0
100
0
0
0
0
75
0
25
0
0
100
0
0
0
0
91.7
0.0
8.3
0.0
0.0
(4) the highest pH in the samples collected at the end
of the dry season was related to an EC far lower
than that of the lakes with pH > 9.
These data enable us to visualise the existence of
two independent processes that increase the lakes’ pH,
as proposed by Zavarzin (2002): (1) increasing salinity
through evaporation (directly associated to the degree
of isolation of the lake from the phreatic recharge); and
(2) the increasing density of organisms (directly associated to the high proliferation rate of phytoplankton).
The BA21 lake at the beginning of the dry season had
a high pH and the highest EC of the sampled group.
With the EC increasing towards the highest value found
in all the campaigns (and therefore the highest salinity),
the isolation of this lake and the favourable conditions
for an intense phytoplankton bloom are clearly evident.
This bloom was probably partly responsible for the increase in pH, because the EC increased 2.3 fold (a simAn Acad Bras Cienc (2011) 83 (2)
400
TEODORO I.R. ALMEIDA et al.
TABLE V
Number of genera and species described by salinity of water classes adopted (G = Genus; sp = species).
Class of water (all the lakes)
Class of organisms
Cyanobacteria
Chlorophyceae
Bacillariophyceae
Cryptophyceae
Dinophyceae
Chrysophyceae
Euglenophyceae
All the organisms
Freshwater
Low to average
High
Very high
salinity
salinity
salinity
Hypersaline
G
8
9
15
23
6
sp
8
13
20
27
7
G
25
27
16
0
6
sp
33
44
17
0
6
G
5
4
–
6
0
sp
5
4
0
6
0
G
2
3
9
0
3
sp
2
3
9
0
3
G
1
2
0
1
0
sp
1
2
0
1
0
G
1
1
0
0
0
sp
1
1
0
0
0
G
3
3
0
3
0
sp
3
3
0
3
0
G
45
49
40
33
15
sp
53
70
46
37
16
TABLE VI
Number of species of phytoplanktonic organisms observed in the
lake samples from the Rio Negro farm and the relative percentage
of cyanobacteria. Sampling was done in August 2007.
Class of water
All
% Species of
species
cyanobacteria
Freshwater (four lakes)
52
15
Low to average salinity (three lakes)
69
19
High salinity (five lakes)
46
43
Very high salinity (four lakes)
37
73
Hypersaline (two lakes)
16
44
TABLE VII
Species of phytoplankton observed in the lake samples from the Barranco Alto farm
and the relative percentage of cyanobacteria. The first sample collection was done
in July 2008 and the second in October 2008.
Class of water
All species
1st sampling
% Species of cyanobacteria
2nd sampling
1st sampling
2nd sampling
Freshwater
11
9
9
44
Low to average salinity
28
31
25
29
High salinity
18
24
22
58
Very high salinity
15
17
87
100
Hypersaline
9
12
44
44
An Acad Bras Cienc (2011) 83 (2)
401
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
TABLE VIII
Density of organisms, EC and pH of the samples of October 2008.
The highest pHs are related to the highest density of organisms in extreme dryness
(bold characters and grey lines). Data ordered by pH of the second sampling.
Density of organisms
(org.mL−1 )
Lakes
BA37
BA2
BA31
BA3
BA36
BA5
BA35
BA7
BA9
BA25
BA16
BA21
BA24
First sampling
61,726
23,493
630
27,178
148
354,695
51,795
204,986
23,402
18,759
1,032,990
123,256
401,862
Second sampling
119,019
13,727
35,141
144,697
284
12,319
212,641
257,568
95,077
6,909
2,763,854
10,443,842
1,020,323
ilar pattern to the average of all the lakes – 2.1 times),
whereas the density of organisms increased 85 fold.
This suggests that two processes act to increase the
pH and alkalinity: one geochemical and other biogenic.
Analysis of the densities of organisms in lakes BA16,
BA21 and BA24 show that the latter had the highest
pH of the group and the lowest density of organisms.
The data could indicate that, in this case, the alkalinisation was simply dominated by physicochemical processes, such as evidenced by the geochemical imbalance
in evaporation. Another possibility is that when the pH
attain the peak of 9.8, there are a fall in CA activity,
reducing the productivity of these organisms. Both hypotheses could explain a small increase in the cyanobacterial population in the most alkaline lake, with a
pH > 10, but the latter seems more convincing because
the EC of lake BA24 was not particularly high.
Arranging the data according to the population
density of the organisms, the six lakes with density
> 150,000 org.mL−1 coincided with the five lakes with
the highest pHs and with five of the eight lakes with a
EC > 750 gS.cm−1 , indicating a significant correlation
(Table IX). By contrast, the lake with the highest EC
had one of the lowest densities of organisms, and one
of the lakes with the highest density of organisms had
First sampling
EC
pH
µS.cm−1
1750
113
95
172
940
3185
780
2932
4140
710
3618
7188
1591
9.28
7.09
6.5
7.77
8.89
9.3
9.09
9.31
9.44
9.28
9.46
9.33
9.38
Second sampling
EC
pH
µS.cm−1
3940
161
170
229
2116
4567
2032
5641
6607
2317
8410
16360
3976
7.98
8.35
8.69
8.77
9.19
9.21
9.45
9.6
9.67
9.68
9.77
9.78
10.06
one of the lowest ECs, an evidence that phytoplankton blooms are not strictly dependent on EC (or salinity). However, ordering the data by pH, the five highest pHs were associated with five of the six highest microorganism densities. Finally, in these two groups of
independent data (the lakes from the Rio Negro and Barranco Alto farms), the highest densities were linked to
the highest salinities, suggesting that the most intense
blooms occur in those lake waters more isolated from
the phreatic zone. The fact that all the studied lakes with
pH > 9.0 in October had very high salinity or hypersalinity suggests a causal relationship between the processes
of isolation and alkalinisation of these lakes.
In the August 2007 fieldwork data (Table X), there
is an evident correlation between the chlorophyll and
pheophytin pigments with pH. Considering that only
cyanobacteria have pheophytin and that organisms of
other classes were described in all the classes of water, the sum of these two pigments was considered
more representative of the biogenic contribution to
increased pH.
The data concerning pigments in the samples of
the fieldworks of 2008 are clear (Table XI). In the two
sample collections, there were two contrasting groups
of samples: those with low pigment levels and those
An Acad Bras Cienc (2011) 83 (2)
402
TEODORO I.R. ALMEIDA et al.
TABLE IX
Density of organisms, EC and pH of the August 2007 sampling. The data are
ordered by pH on the left and by EC on the right. The highest pHs are related to
the highest density of organisms, and there is a greater independence from EC.
The data showing the higher density of organisms, pH and EC are in bold characters.
Density of
Lake
organisms
pH
org.mL−1
Density of
EC
Lake
µS.cm−1
organisms
pH
org.mL−1
EC
µS.cm−1
RN 3b
300
7.13
110
RN 7b
1100
7.33
27
RN 4b
900
7.17
286
RN 1b
12900
8.11
30
RN 5b
84800
7.32
591
RN 6b
3200
8.28
42
RN 7b
1100
7.33
27
RN 2b
164400
8.52
74
RN 1b
12900
8.11
30
RN 3b
300
7.13
110
RN 6b
3200
8.28
42
RN 4b
900
7.17
286
RN 2b
164400
8.2
74
RN 5b
84800
7.32
591
RN 8s
700
9.03
12593
RN 3s
649500
9.7
2429
RN 2s
2900
9.06
3467
RN 4s
1059
9.37
2798
RN 4s
1059
9.37
2798
RN 1s
150200
9.41
2858
RN 5s
423400
9.4
7156
RN 2s
2900
9.06
3467
RN 1s
15020
9.41
2858
RN 5s
423400
9.4
7156
RN 6s
5914600
9.41
11500
RN 7s
159400
9.51
8572
RN 7s
159400
9.51
8572
RN 6s
5914600
9.41
11500
RN 3s
649500
9.7
2429
RN 8s
700
9.03
12593
TABLE X
Pigments in phytoplankton (chlorophyll a and pheophytin),
pH and EC. Bold characters: samples with pH > 9. The data
are ordered by the sum of the chlorophyll a + pheophytin values.
Lake
RN 4b
Chl a
Pheo
Chl a + pheo
µg.L−1
4.44
4.37
RN 3b
2.22
RN 2b
10.36
pH
EC
µS.cm−1
8.81
7.17
286
6.59
8.81
7.13
110
2.07
12.43
8.52
74
RN 7b
14.06
7.44
21.50
7.33
27
RN 7s
21.90
4.20
26.10
9.51
8572
RN 1b
23.68
7.4
31.08
8.11
30
RN 6b
18.94
15.87
34.81
8.28
42
RN 2s
22.20
15.10
37.30
9.06
3467
RN 5b
22.69
18.06
40.75
7.32
591
RN 4s
29.60
18.75
48.35
9.37
2798
RN 8s
29.6
28.42
58.02
9.03
12593
RN 5s
51.06
10.06
61.12
9.4
7156
RN 3s
231.9
123.8
355.7
9.7
2429
RN 1s
237.9
120.9
358.87
9.41
2858
RN 6s
2836
554.1
3390
9.41
11500
An Acad Bras Cienc (2011) 83 (2)
403
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
TABLE XI
Contents of chlorophyll a, pheophytin, pH and EC of the samples collected in July (first sampling) and October 2008
(second sampling). Both tables are ordered by pH. Bold characters: the samples in which the sum of the
pigment values is significant.
First sampling
Lakes
Chl
Pheo
Chl + Pheo
µg.L−1
Second sampling
pH
EC
µS.cm−1
Lakes
Chl
Pheo
Chl + Pheo
µg.L−1
pH
EC
µS.cm−1
BA31
2.1
1.8
3.9
6.5
95
BA37
20.2
12
32.2
7.98
3940
BA2
38.4
18.8
57.2
7.09
113
BA2
33.5
7.5
41
8.35
161
BA32
30.7
6.9
37.6
7.74
154
BA31
14.7
2.4
17.1
8.69
170
BA3
27.9
6.3
34.2
7.77
172
BA3
34.9
7.4
42.3
8.77
229
BA13
3.5
2.1
5.6
8.69
785
BA36
2.8
–
9.19
2116
BA12A
1.4
2
3.4
8.71
1045
BA5
15.4
7.6
23
9.21
4567
BA36
6
5.2
11.2
8.89
940
BA35
82.3
17.8
100.1
9.45
2032
BA12B
120
26.5
146.5
8.98
1160
BA7
51.6
19.2
70.8
9.6
5641
BA34
162.5
34.2
196.7
9
1001
BA9
−1
−1
−2
9.67
6607
BA35
17.1
3.6
20.7
9.09
780
BA22
25.1
8.1
33.2
9.67
12870
BA22
2594.7
530.1
3124.8
9.25
5357
BA25
18.1
6.8
24.9
9.68
2317
BA25
19.5
4.9
24.4
9.28
710
BA16
2399.4
4895.1
7294.5
9.77
8410
BA37
23.7
3.6
27.3
9.28
1750
BA21
2976
956
3932
9.78
16360
BA5
27.9
8.7
36.6
9.3
3185
BA26
1004.4
1812.8
2817.2
9.85
6857
BA7
25.1
11.5
36.6
9.31
2932
BA24
5003.4
2287.8
7291.2
10.06
3976
BA21
5761.4
1738.2
7499.6
9.33
7188
BA24
3325.7
873.3
4199
9.38
1591
BA9
23
6.8
29.8
9.44
4140
BA16
17.4
7
24.4
9.46
3618
BA14
152.5
28.5
181
9.49
2517
BA26
1735.4
471.5
2206.9
9.5
2671
BA33
4.2
2.2
6.4
9.52
438
with very high levels. In the July sample collection at
the beginning of the dry season, there was no correlation between pigment content and pH, indicating that
the action of the microorganisms during this period did
not significantly influence the pH. For the samples collected in October 2008 at the end of the dry season,
the samples with high pigment content corresponded
to the highest pHs. The interpretation seems to be clear:
the action of the phytoplanktonic organisms to increase
the pH occurs in the dry season, concomitant to the
blooms, as observed.
Evaporation, in an environment with a water deficit, will cause intense salinisation in the lakes isolated
from phreatic recharge. Most of the lakes (those that
remain with fresh water all year round) interact with
the phreatic zone and thereby do not suffer an intense
salinisation. The diversity of the lakes of Nhecolândia
in colouration (in the function of microorganisms), the
presence or absence of sand beaches (the high salinity
of the salinas hinders the growth of Gramineae), the
presence of macrophytes (which do not survive in saline
waters) and the lower topographic level of the salinas
in relation to the neighbouring baías could be explained
by the biogeochemical process presented here.
Chemical analyses of the water sampled in July
and October of 2008 revealed negative values of saturation indexes for amorphous silica in all samples from
the baías (Fig. 2), which indicates undersaturation of
the solutions, and values close to zero for the samples
from the salinas, indicating a predominant condition of
chemical equilibrium between the dissolved and mineral states. Such conditions favour the formation of
amorphous silica, especially during the dry season. The
salinas’ basal substrate, composed of a framework of
An Acad Bras Cienc (2011) 83 (2)
404
TEODORO I.R. ALMEIDA et al.
Fig. 2 – Stability of pH × amorphous silica (left) and quartz (right) diagram. Modified from Freeze and Cherry’s (1971).
quartz sand and a cement of amorphous silica, is extremely impermeable. This promotes hydraulic isolation of the lake from the shallow and locally confined
aquifer waters. Figure 2 also indicates that the amorphous silica was in chemical equilibrium with the water samples collected from salinas in July 2008, at the
beginning of the dry season. Samples taken in October
2008 (at the end of the dry season) had a higher content of total dissolved solids, but lower concentrations
of dissolved silica, as well as relatively lower saturation
of amorphous silica, indicating that an removal of silica
from the solution to the solid phase, during the monitoring period, probably occurred.
According Freeze and Cherry’s (1971) data, the
saturation indexes for quartz have positive values (Fig.
2), both for salinas and baías samples (except for three
baías samples), indicating that the mineral is mostly
not dissolved. This observation is apparently discordant
with the hypothesis that the geochemical erosion of
quartz in salinas would explain their lower altitudes relative to these from hyposaline lakes, although the quartz
dissolution may occur in physicochemical conditions
not sampled in the survey, as solutions that precipitate
amorphous silica in the sand of the salinas bottom. Furthermore, the adopted model explains the data for all
the various types of observations made in the study.
These include the relative altitude of the saline and
hyposaline lakes, the ratios of stable isotopes of O
and H, the differences in salinity and the origin of the
silica in solution and, in images from scanning elecAn Acad Bras Cienc (2011) 83 (2)
tron microscopy of the sediments below salinas, amorphous silica in the inter-grain spaces of the sediments
under saline-alkaline lakes, corrosion figures at quartz
grains and irregular grains surfaces in perfectly adjusted
contact to each other. The authors have no alternative
model to explain all the data from seven years of research in the region.
CONCLUSION
This paper presents an original interpretation of the
origin of the diversity of Nhecolândia lakes, based on
both geochemical and biogenic processes. The poverty
in Ca2+ in the regional waters determines an imbalance
of the calcium cycle, because this ion is responsible for
maintaining the neutral pH of most surface water on
Earth. We propose that this geochemical process was the
first to increase the alkalinity of these lakes, according to
2−
a shift in the balance in the system CO2 / HCO−
3 / CO3
2−
to CO3 because of the inability to precipitate CaCO3 .
The phytoplankton, mainly cyanobacteria, help to raise
the pH by consuming inorganic carbon in the form of
CO2 and, markedly, HCO−
3 (which predominates in the
solution from pH > 6), and by excreting OH− .
Originally the water in the lakes should have been
fresh, lacking a basis for high salinity. During the evolution of these lakes, the biogeochemical process raised
the pH of the water, facilitating the dissolution of quartzose sand and silt. The silica-rich water (possibly as
H4 SiO4 ) penetrated the sediments below the lake bottoms, where amorphous silica was precipitated between
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
the clasts. This precipitation could be caused by excessive salinity (during extreme droughts) or drops in
pH (due to contact with the water table). The repetition of this process, including the dissolution of the
fraction of amorphous silica precipitated at the surface
and of additional amounts of quartz (sand and silt),
gradually increases the isolation of the lakes due to the
precipitation of amorphous silica, which acts as a cement between the grains of sand, allowing the generation of high-salinity waters. Note that this repeated process will lead to a progressive lowering of the bed of
the saline-alkaline lakes. The limit for this lowering may
be the groundwater level in extreme drought, which explains the horizontal bottom of the saline-alkaline lakes.
ACKNOWLEDGMENTS
The authors are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP – Process 06/
61052-4) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – Process 483272/
2007-8) for financing the project. Thanks to the landlords of the Barranco Alto farm, Marina Schweizer and
Lucas Leuzinger, for their enormous support and hospitality in the field.
RESUMO
O Pantanal da Nhecolândia é o maior e mais diversificado
campo de lagos da região tropical do planeta, com cerca de
10.000 lagos de variadas salinidade, pH, alcalinidade, cor, fisiografia e atividade biológica dispostos em uma área de
24.000 km2 . Os lagos hipossalinos têm pH variável, baixa alcalinidade, macrófitas e baixa densidade de fitoplâncton. Os
lagos salinos tem pH acima de 9 ou 10, elevada alcalinidade,
alta densidade de fitoplâncton e praias de areia. A causa da
diversidade desses lagos é uma questão ainda em aberto que
é abordada nesta pesquisa. Propõe-se como principal causa
um processo híbrido, geoquímico e biológico, baseado em
(1) clima com um déficit hídrico importante e pobreza em
Ca2+ na água superficial e do freático e (2) na elevação do
pH durante florações de cianobactérias. Estes dois aspectos
desestabilizam a tendência geral de pH neutro para as águas
superficiais da Terra. Este desequilíbrio resulta em aumento
do pH e dissolução da areia quartzosa do fundo dos lagos
salino-alcalinos. Durante secas extremas há precipitação de
sílica amorfa nos espaços inter-granulares dos sedimentos de
405
fundo destes lagos, aumentando seu isolamento do freático.
O artigo discute este processo biogeoquímico, à luz de dados
físico-químicos, químicos, fitoplânctonicos e de altimetria de
precisão.
Palavras-chave: Pantanal, lagos alcalinos, lagos salinos, cianobactérias, processos de alcalinização.
REFERENCES
A LMEIDA FFM. 1945. Geologia do sudoeste Matogrossense.
Bol DNPM/DGM 116: 1–118.
A LMEIDA TIR, PARANHOS F ILHO AC, ROCHA MM,
S OUZA GF, S IGOLO JB AND B ERTOLO RA. 2009. Um
estudo sobre as diferenças de altimetria do nível da água
de lagoas salinas e hipossalinas no Pantanal da Nhecolândia: um indicativo de funcionamento do mega sistema
lacustre. Geociências 28: 401–415.
A LMEIDA TIR, S ÍGOLO JB, F ERNANDES E, Q UEIROZ
N ETO JP, BARBIERO L AND S AKAMOTO AY. 2003.
Proposta de classificação das lagoas da Baixa Nhecolândia-MS com base em sensoriamento remoto e dados de
campo. R Bras Geoc 33: 83–90.
A PHA – A MERICAN P UBLIC H EALTH A SSOCIATION . 1995.
Standard methods for the examination of water and wastewater. Springfield, USA, Byrd Prepress.
A SSINE ML. 2004. Quaternary of the Pantanal, west-central
Brazil. Quatern Int 114: 23–34.
A SSUMPÇÃO M. 1998. Focal mechanisms of small earthquakes in the southeastern Brazilian shield: a test of stress
models of the South American plate. Geophys J Int 133:
490–498.
BARBIERO L, Q UEIROZ N ETO JP, C IORNEI G, S AKAMOTO
AY, C APELLARI B AND F ERNANDES E. 2002. Geochemistry of water and ground water in the Nhecolândia,
Pantanal of Mato Grosso, Brazil: Variability and associated processes. Wetlands 22: 528–540.
BARBIERO L, R EZENDE F ILHO A, F URQUIM SAC, F URIAN
S, S AKAMOTO AY, VALLES V, G RAHAM VRC, F ORT
M, F ERREIRA RPD AND Q UEIROZ N ETO JP. 2008. Soil
morphological control on saline and freshwater lake hydrogeochemistry in the Pantanal of Nhecolândia, Brazil.
Geoderma 148: 91–106.
C OSTA MPF AND T ELMER KH. 2007. Mapping and monitoring lakes in the Brazilian Pantanal wetland using synthetic aperture radar imagery. Aquat Conservat Mar
Freshwat Ecosyst 17: 277–288.
D E -L AMONICA -F REIRE EM AND H ECKMAN CW. 1996.
The Seasonal succession of biotic communities in wetlands of the tropical wet-and-dry climatic zone: iii. The
An Acad Bras Cienc (2011) 83 (2)
406
TEODORO I.R. ALMEIDA et al.
algal communities in the Pantanal of Mato Grosso, Brazil,
with a comprehensive list of the known species and revision of two desmid taxa. Int Rev ges Hydrobiol Hydrogr
81: 253–280.
D UCKWORTH AW, G RANT WD, J ONES BE AND VAN
S TEENBERGEN R. 1996. Phylogenetic diversity of soda
lake alkaliphiles. FEMS Microbiology Ecol 19: 181–191.
E STEVES FA. 1998. Fundamentos de Limnologia. Rio de
Janeiro, Brazil, Interciência.
F REEZE A AND C HERRY J. 1971. Groundwater. Englewood
Cliffs, USA, Prentice Hall.
F URQUIM SAC, G RAHAM RC, BARBIERO L, Q UEIROZ
N ETO JP AND VALLÈS V. 2008. Mineralogy and genesis of smectites in an alkaline-saline environment of
Pantanal wetland, Brazil. Clays Clay Miner 56: 580–596.
F URQUIM SAC, G RAHAM R, BARBIERO L, Q UEIROZ
N ETO JP AND V IDAL -T ORRADO P. 2010. Soil mineral
genesis and distribution in a saline lake landscape of the
Pantanal wetland, Brazil. Geoderma 154: 518–528.
G ALVÃO LS, P EREIRA F ILHO W, A BDON MM, N OVO
EMLM, S ILVA JSVE AND P ONZONI FJ. 2003. Spectral reflectance characterization of shallow lakes from the
Brazilian Pantanal wetlands with field and airborne hyperspectral data. Int J Remote Sens 24: 4093–4112.
J ONES BE, G RANT WD, D UCKWORTH AW AND OWEN SON GG. 1998. Microbial diversity in soda lakes. Extremophiles 2: 191–200.
K UPRIYANOVA E, V ILLAREJO A, M ARKELOVA A, G ERA SIMENKO L, Z AVARZIN G, S AMUELSSON G, L OS DA
AND P RONINA N. 2007. Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology 153: 1149–1156.
M C C ONNAUGHEY TA AND W HELAN J F. 1997. Calcification generates protons for nutrient and bicarbonate uptake. Earth-Sci Rev 42: 95–117.
M C C ULLOUGH JD AND JACKSON DW. 1985. Composition
and productivity of the benthic macroinvertebrate community of a subtropical reservoir. Int Rev Ges Hydrobiol
Hydrogr 70: 221–235.
M EDINA -J ÚNIOR PB AND R IETZELER AC. 2005. Limnological study of a Pantanal saline lake. Braz J Bio 65:
651–659.
M ELACK JM AND K ILHAM P. 1974. Photosynthetic rates
of phytoplankton in East African alkaline, saline lakes.
Limnol Oceanogr 19: 743–755.
N USH EA. 1980. Comparisons of different methods for chlorophyll and phaepigment. Arch Hydrobiol 14: 14–36.
O DUOR SO
AND
S CHAGERL M. 2007. Temporal trends of
An Acad Bras Cienc (2011) 83 (2)
ion contents and nutrients in three Kenyan Rift Valley
saline-alkaline lakes and their influence on phytoplankton
biomass. Hydrobiologia 584: 59–68.
O LIVEIRA MD AND C ALHEIROS DF. 2000. Flood pulse influence on phytoplankton communities of the south Pantanal floodplain, Brazil. Hydrobiologia 427: 101–112.
P OR FD. 1995. The Pantanal of Mato Grosso (Brazil). World’s
Largest Wetlands. London, UK, Kluwer Academic Publisher.
S ANTOS KRS, S AKAMOTO AY, N ETO MJ, BARBIERO L
AND Q UEIROZ N ETO JP. 2004. Ficoflora do Pantanal da
Nhecolândia, MS, Brasil: um levantamento preliminar em
três lagoas alcalinas e uma salitrada. In: S IMPÓSIO SO BRE R ECURSOS NATURAIS E S ÓCIO - ECONÔMICOS DO
PANTANAL, 4, Corumbá, Brazil. Proceedings... Brasília:
EMBRAPA, 2004, CD ROM.
S ANTOS KRS AND S ANT ’A NNA CL. 2010. Cianobactérias
de diferentes tipos de lagoas (“salina”, “salitrada” e “baía”)
representativas do Pantanal da Nhecolândia, MS, Brasil.
Rev Bras Bot 33: 61–83.
S ERGEEV VN, G ERASIMENKO LM AND Z AVARZIN GA.
2002. The Proterozoic history and present state of cyanobacteria. Microbiologia 71: 623–637.
S HAPIRO J. 1990. Currents beliefs regarding dominance by
blue-greens: the case of the importance of CO2 and pH.
Verh Internat Verein Theor Angew Limnol 24: 38–54.
S ILVA JSV, A BDON MM, B OOCK A AND S ILVA MP. 1998.
Delimitation of the Brazilian Pantanal and its sub-regions.
Braz J Agric Res 33: 1703–1713.
S ILVA LHS, DAMAZIO CM AND I ESPA AAC. 2008. Identificação de Cianobactéricas em Sedimentos da Lagoa
Pitanguinha, Estado do Rio de Janeiro, Brasil. Anu Inst
Geoc 31: 11–16.
S MITH KS, JAKUBZICK C, W HITTAM TS AND F ERRY JG.
1999. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. PNAS 96: 15184–15189.
T HOMPSON JB AND F ERRIS FG. 1990. Cyanobacterial precipitation of gypsum, calcite, and magnesite from natural
alkaline lake water. Geology 18: 995–998.
T ILMAN DL. 1977. Resource competition between phytoplanktonic algae: an experimental and theoretical approach. Ecology 58: 338–348.
USSL – U NITED S TATES S ALINITY L ABORATORY. 1954.
Diagnosis and improvement of saline and alkali soils.
Washington, USA, U.S. Dept Agricult.
U SSAMI N, S HIRAIWA S AND D OMINGUEZ JML. 1999.
Basement reactivation in a sub-Andean foreland flexural
bulge: the Pantanal wetland, SW Brazil. Tectonics 18:
25–39.
BIOGEOCHEMICAL PROCESSES AND PANTANAL LAKES DIVERSITY
U THERMOHL H. 1958. Zur Vervolkommung der quantitative Phytoplankton-Methodik. Mitteilungen. Internat
Verein Limnol 9: 1–38.
V ISSCHER PT, R EID PR, B EBOUT BM, H OEFT SE, M AC I NTYRE IG AND T HOMPSON J R JA. 1998. Formation of
lithified micritic laminae in modern marine stromatolites
(Bahamas); the role of sulfur cycling. Am Mineral 83:
1482–1493.
407
W ESTALL F. 2005. Life on the early earth: a sedimentary
view. Science 308: 366–367.
Z AVARZIN GA. 2002. Microbial geochemical calcium cycle.
Microbiologia 71: 1–17.
An Acad Bras Cienc (2011) 83 (2)