paleolimnologically inferred eutrophication of a shallow ......e-mail: [email protected] a....
TRANSCRIPT
ORIGINAL PAPER
Paleolimnologically inferred eutrophication of a shallow,tropical, urban reservoir in southeast Brazil
Sandra Costa-Boddeker • Helen Bennion • Tatiane Araujo de Jesus •
Ana Luiza S. Albuquerque • Rubens C. L. Figueira •
Denise de C. Bicudo
Received: 11 July 2011 / Accepted: 16 August 2012 / Published online: 4 September 2012
� Springer Science+Business Media B.V. 2012
Abstract We studied the eutrophication history of a
tropical shallow reservoir in the Sao Paulo metropol-
itan region, southeast Brazil. We analyzed grain size,
geochemistry, diatom assemblages, and land-use
records in a sediment core from the reservoir to infer
its trophic state history during the last *110 years
(1894–2005). Eighty diatom species were observed in
the core and shifts in the relative abundances of
planktonic and benthic taxa indicate major limnolog-
ical changes associated with complex interactions
between hydrologic factors and eutrophication.
Discostella stelligera was associated with deforesta-
tion and water physical changes whereas Aulacoseira
granulata, a species abundant throughout the core,
was mostly associated with high flux conditions and
erosion events, regardless of trophic state. Eutrophi-
cation was triggered by construction of the city zoo
(1958) and installation of the Sao Paulo State Depart-
ment of Agriculture (1975) within the Garcas
watershed, and increasing loads of untreated sewage
from these institutions. The data suggest that deteri-
oration in water quality began after *1975 and
markedly accelerated after *1990. The reservoir has
been hypereutrophic since 1999. Steady increases in
geochemical proxies for trophic state, along with a
decrease in C/N ratios, indicated higher nutrient
Electronic supplementary material The online version ofthis article (doi:10.1007/s10933-012-9642-1) containssupplementary material, which is available to authorized users.
S. Costa-Boddeker � D. de C. Bicudo (&)
Department of Ecology, Instituto de Botanica, Av. Miguel
Stefano, 3687, 04301-012 Sao Paulo, SP, Brazil
e-mail: [email protected]
S. Costa-Boddeker
e-mail: [email protected]
H. Bennion
Department of Geography, Environmental Change
Research Centre, University College London,
London, UK
e-mail: [email protected]
T. A. de Jesus
Centro de Engenharia, Modelagem e Ciencias Sociais
Aplicadas, Universidade Federal do ABC, Santo Andre,
SP, Brazil
e-mail: [email protected]
A. L. S. Albuquerque
Departamento de Geoquımica, Instituto de Quımica,
Universidade Federal Fluminense, Niteroi,
Rio de Janeiro, Brazil
e-mail: [email protected]
R. C. L. Figueira
Oceanographic Institute of Sao Paulo University,
Sao Paulo, SP, Brazil
e-mail: [email protected]
123
J Paleolimnol (2012) 48:751–766
DOI 10.1007/s10933-012-9642-1
concentrations and the prevalence of autochthonous
production towards the core top. Appearance of
Achnanthidium catenatum *1993 highlighted the
onset of a marked eutrophication phase. The sub-
sequent dominance of Planothidium rostratum and
Cyclotella meneghiniana suggested a sharp shift to a
hypereutrophic state since 1999. Land-use history
proved valuable for validating the chronology and
interpreting anthropogenic impacts. Multi-proxy anal-
ysis of the sediment record provided an effective tool
for tracking ecological shifts in the reservoir ecosys-
tem. This study provides the first reconstruction of
lake eutrophication history in Brazil and highlights the
importance of hydrological/physical changes as driv-
ers of diatom assemblage shifts in reservoirs, which
may confound trophic state inferences based on shifts
in the planktonic/benthic diatom ratio.
Keywords Diatoms � Eutrophication �Geochemical proxies � Multiple stressors �Ecological shifts � Land-use change
Introduction
Eutrophication is a well documented environmental
problem that has caused deterioration of water quality
in lakes throughout the world. It has been recognized as
a global problem for decades and in some lakes for
centuries (Findlay et al. 1998). Generally, eutrophica-
tion is associated with increasing human activity in lake
catchments and elevated loading of the key nutrients,
nitrogen and phosphorus, from domestic, agricultural or
industrial sources. In urban lakes, water quality dete-
rioration can be relatively rapid and intense as a result
of land use in the catchment (Johnes 1999). Shallow
lakes are particularly susceptible to eutrophication, and
feedback mechanisms are especially strong in tropical/
subtropical ecosystems, thereby intensifying system
resistance to restoration strategies (Bicudo et al. 2007).
According to Lewis (2000), tropical lakes could
seriously decline in their usefulness as sources of water
supply, commercial production of species and recrea-
tion, if there are no effective programs for the protection
and management of such ecosystems.
Knowledge of the natural baseline condition of an
ecosystem, prior to disturbance, is fundamental to the
design of effective recovery strategies, as it allows a
realistic target to be set and provides a benchmark
against which managers can evaluate the degree to
which their restoration efforts are successful (Bennion
and Battarbee 2007; Dixit et al. 2007; Bennion et al.
2011). Long-term monitoring data are important for
understanding the complexity of environmental
change in time and space, but sadly, they are rarely
available (Battarbee et al. 2005). Lake sediments,
however, can preserve the environmental history of a
drainage basin and provide valuable information about
lake response to external influences (Smol 2008).
Therefore, in the absence of long-term-monitoring
data, biological indicator groups preserved in lake
sediments can be employed to reconstruct lake eutro-
phication history. Diatom assemblages, in particular,
have been successfully and widely used in studies of
trophic status (Bennion et al. 2004; Hall and Smol
2010; Juttner et al. 2010; Kirilova et al. 2010).
Nonetheless, very few paleolimnological studies have
used diatoms to track eutrophication in tropical lakes
(Stoof-Leichsenring et al. 2011). Indeed, there is only
one such study in South America, albeit not within a
tropical region, carried out in Laguna de San Pedro,
Chile (Cruces et al. 2001). Moreover, the use of
diatoms for paleolimnological studies in reservoirs has
been very scarce worldwide (Liu et al. 2012).
This study aimed to (a) reconstruct qualitatively the
eutrophication history of a tropical urban shallow
reservoir over the last century, encompassing the pre-
industrial period in Brazil, and (b) contribute to the
understanding of the interplay between anthropogeni-
cally induced hydrological/physical changes and eutro-
phication on diatom assemblage shifts over time. The
study focuses on Garcas Reservoir, in the city of Sao
Paulo, which was used for water supply at the beginning
of the last century and is presently hypereutrophic. The
system has been monitored since 1997 (Bicudo et al.
2007; Crossetti et al. 2008), but there are no data
available for the period prior to eutrophication. This
study provides the first attempt to investigate eutrophi-
cation from a paleolimnological perspective in Brazil.
Moreover, to our knowledge, the interplay between
hydrological/physical changes and eutrophication, and
how they influence diatoms in tropical shallow lake/
reservoir ecosystems, has not been previously explored.
Study site
Garcas Reservoir is located in the Biological Reserve
of Ipiranga Headsprings State Park, known as PEFI,
752 J Paleolimnol (2012) 48:751–766
123
in the city of Sao Paulo, southeast Brazil (23�38.080Sto 23�40.180S; 46�36.480W to 46�38.000 W). This
reserve contains one of the largest remnants of
Atlantic Forest in a densely inhabited (*17 million
people) urban area (Fig. 1). The surface area and mean
altitude of the park are 526 ha and 798 m a.s.l.,
respectively. Climate in the area is tropical (Bicudo
et al. 2007). Presently, the reserve includes predom-
inantly Atlantic Forest remnants, 24 headsprings, nine
artificial lakes, as well as the city zoo, the Sao Paulo
Botanical Garden, research institutions, and the Sao
Paulo State Department of Agriculture and Provision-
ing headquarters. It is surrounded by the Sao Paulo
metropolitan urban region.
Garcas Reservoir (23�380S, 46�370W) originated
from a former water supply reservoir (Campanario
Reservoir) constructed in 1894 by damming Cam-
panario creek to meet the increasing demand for
drinking water, and was used for this purpose until
1928. Starting in *1917, the original reservoir was
split into five smaller waterbodies, and Garcas Reser-
voir became the main system. It has a catchment area
of 2.62 km2 including forested and urban areas, a
surface area of 88,156 m2, mean depth and maximum
depth of 2.1 and 4.7 m, respectively, a mean residence
time of 71 days, and is classified as a warm, polymic-
tic and discontinuous system (Bicudo et al. 2007).
Since 1958, the reservoir received untreated sewage
loads from the city zoo (inflows 3 and 5, Fig. 1) and in
the latter half of the 1970s a further effluent source
from the Sao Paulo State Department of Agriculture
and Provisioning headquarters (inflow 7, Fig. 1)
(Bicudo et al. 2007). In 1997, a monthly monitoring
program of the water quality and the phosphorus and
nitrogen loads to the reservoir was initiated. Based on
this temporal series of 8 years (1997–2004), Bicudo
Fig. 1 Location of the State
of Sao Paulo in Brazil and
the Sao Paulo metropolitan
urban region (RMSP) and
municipality (shaded area).
In the square, the Garcas
Reservoir surrounded by the
Ipiranga Headsprings State
Park (PEFI) Biological
Reserve. Reservoir
bathymetric map shows the
core sampling site
(indicated by a star);
numbers 1–7 refer to the
main inflows
J Paleolimnol (2012) 48:751–766 753
123
et al. (2007) characterized two contrasting limnolog-
ical phases. During 1998–1999 a pronounced prolif-
eration of water hyacinths (Eichhornia crassipes Mart.
Solms-Laub) occurred, occupying 40–70 % of the
reservoir surface area. Since the end of 1999, and
triggered by the mechanical removal of plants, the
reservoir abruptly shifted to a stable degraded state
with permanent cyanobacterial blooms (Microcystis
aeruginosa (Kutz.) Kutz., M. panniformis J. Komarek
et al. and/or Cylindrospermopsis raciborskii (Wol.)
Seen. et Subba Raju) and hypereutrophic nutrient
concentrations (Table 1). Biological feedback mech-
anisms were driven by cyanobacterial blooms. The
blooms enhanced water stability and increased bio-
mass decomposition in the aphotic zone, thereby
extending the period of bottom anoxia and in turn
creating conditions suitable for sediment P release
(Bicudo et al. 2007). A sharp phytoplankton biodiver-
sity loss has occurred since that time (Crossetti et al.
2008). In terms of macrophytes, the reservoir supports
one stand of E. crassipes, isolated with metal frames
and wire close to the entry point of zoo effluent, and no
submerged vegetation.
Materials and methods
Core sampling
In July 2005, four parallel sediment cores were hand
collected by divers at the deepest point in the reservoir
(Fig. 1) using a Plexiglas tube (8 cm diameter 9
100 cm long). Two cores were archived and the
remaining two, LG05-03 (65 cm long) and LG05-04
(70 cm long) were sliced in the field at 1 cm intervals,
and sub-samples were subsequently used for analysis
of the multiple sediment variables and geochronology.
LG05-03 was used for total phosphorus (TP), total
organic carbon (TOC) and total nitrogen (TN) anal-
yses, and LG05-04 was used for diatom, water content
and geochronology analyses. Both cores were used for
grain size analyses and to describe lithological char-
acteristics (color and texture).
Geochronology
A total of 17 samples representing the whole length of
the LG05-04 core was radiometrically measured for210Pb and 226Ra activity by direct alpha–beta assay in
the Environmental Geochemistry Laboratory (Federal
University of Sao Carlos, Sao Paulo, Brazil) using a
Canberra Tennelec series 5-XLB—console based
automatic ultra-low background alpha/beta counting
system of argon methane (Cazotti et al. 2006). 210Pb
was determined indirectly by counting beta emission
of 210Bi (Eb = 1170 keV), its radioactively daughter
in secular equilibration. 226Ra was quantified by its
alpha emission (Ea = 4784 keV), after chemical
extraction and separation by a strong anionic resin
(Dowex 1x8). Alpha activity was determined after
20 days (226Ra and its ‘‘descendents,’’ i.e. alpha
emissions, 222Rn, 218 Po, 214Po and 210Po) and beta
activity after 10 days to allow radioactive equilibra-
tion.210Pb chronologies and sedimentation rate were
calculated using the Constant Initial Concentration
(CIC) model by linear regression between excess210Pb and core depth (Appleby and Oldfield 1978),
with an estimated error of 5 %. The total mass of
solids (Ms) was determined by subtracting the water
content for each sample, as follows:
Table 1 Means of
limnological variables in the
Garcas Reservoir and nutrient
loadings during 1997–1998
(n = 16): before water
hyacinth outbreak, 1998–1999
(n = 16): water hyacinth
outbreak, 2000–2004 (n = 48):
after macrophyte removal
(Bicudo et al. 2007)
Variables 1997–March/1998 April/1998–September/1999 2000–2004
Surface chlorophyll-a (lg L-1) 75 41 252
Surface TP (lg L-1) 118 75 310
Surface TN (lg L-1) 845 1,189 5,738
Secchi transparency (m) 0.6 1.0 0.2
Surface pH 6.95 6.68 8.33
Bottom SRP (lg L-1) 12.0 6.0 155.0
TP loadings (kg month-1) 352 510 534
TN loadings (kg month-1) 691 2,073 3,985
754 J Paleolimnol (2012) 48:751–766
123
Ms ¼Dsð1� UÞ � pD2
4� h
UðDs � 1Þ þ 1
where Ds: density of solids, obtained with a picnometer
(g/cm3), U: humidity content, obtained by weighing a
known volume of sediment before and after oven
drying (100 �C) (%), D: internal diameter of Plexiglas
tube (cm), h: thickness of sediment slice (cm).
Documentary information was also collated (Sao
Paulo State documents, museum and library archives,
maps, conversations with local people and published
papers) to track changes in land use in the catchment
and in the limnological features of the reservoir, and to
assist with validation of the geochronology.
Analytical methods
TOC and TN concentrations were analyzed in a Carlo
Erba EA 1110 elemental analyzer. Sediment samples
were precisely weighed (0.1 g) in tin capsules. Hydro-
chloric acid (1.2 mol L-1) was used for inorganic carbon
removal (Hedges and Stern 1984). Quantification was
performed using calibration curves (r [0.999) and
cystine as a standard. Precision was ±3.9 % for TOC
and ±7.4 % for TN, based on the coefficient of variation
of replicate analysis (n = 10) of a reference material
(PACS-2/NRCC). Limit of detection was calculated as
0.01 % for TN. Total phosphorus (TP) was analyzed by
the colorimetric method (Valderrama 1981) after acid
digestion with nitric and perchloric acid (Andersen
1976). Grain size determination was performed by a
laser granulometer CILAS 1064 L (Blott and Pye 2001).
Diatom analysis
Diatom slides were prepared following standard
techniques (Battarbee et al. 2001a). Whenever possi-
ble, approximately 500 valves were counted per slide.
Counts were made using a Zeiss� microscope
(Axioskop 2 plus Type) with oil immersion objective
(1,0009 magnification). Species abundances were
expressed as percentages. The species were identified
according to classic works and specific floras (Met-
zeltin et al. 2005; Metzeltin and Lange-Bertalot 2007).
Data analysis
Major changes in the diatom assemblages over time
were determined by multivariate statistical analyses.
Principal component analysis (PCA) was used to
ordinate diatom abundances in relation to time. Before
computation, variables were log transformed (x ? 1).
Broken-stick eigenvalues were used to define the
number of interpretable axes (Jackson 1993). Data
transformation and PCA were carried out using
PCORD version 4.10 for Windows (McCune and
Mefford 1999).
Diatom assemblage zones (DAZ) were identified by
their distribution throughout the core and constrained
incremental sum of squares (CONISS) implemented by
the programs TILIA and TILIAGRAPH (Grimm 1991).
Stratigraphic changes were plotted for the abundant
diatom species (C5 %), as well as for geochemical TP,
TN, TOC percentages and C/N ratios, using the C2
program, version 1.5 (Juggins 2003).
Results
210Pb chronology
Application of the CIC model was considered appro-
priate for deriving the chronology, given the strong
correlation (r = 0.91) between natural log 210Pbatm
activity and cumulative mass (Fig. 2). Moreover the
derived dates were in agreement with the watershed
land use history and the recent limnological features of
Garcas Reservoir, i.e. monitoring data since 1997
(Table 2). Several events were highlighted as chrono-
logical markers: (1) reservoir construction in *1894,
(2) deforestation of a large area in *1975, indicated
by diatoms (see ‘‘Discussion’’), (3) a layer comprised
of 100 % very fine sand, corresponding to an erosion
episode of one of the reservoir margins in *1991 and
(4) water hyacinth proliferation in 1998 and the shift
from a eutrophic to a hypereutrophic state in 1999. The210Pb dates indicate that the 65-cm-long core repre-
sents sediment deposited over the last *110 years.
Lithology and grain size
Both cores (LG05-03 and LG05-04) consisted mostly
of light grey to black clay sediments from 52 cm
(*1947) to the top. The base consisted of yellow to
light brown sandy material. Grain size composition
showed that coarse silt (16 lm) and very coarse silt
(30 lm) prevailed throughout most of the record,
whereas the core base consisted of fine sand (125 lm)
J Paleolimnol (2012) 48:751–766 755
123
Fig. 2 Unsupported 210Pb
versus cumulative mass
(g cm-2) in core LG05-04
Table 2 210Pb dates for the Garcas Reservoir core LG05-04 and key historical events as recorded by land use records and monitoring
data
Depth (cm) Chronology Sedimentation rate Key historical events
g cm-2 Date AD Age (years) (g cm-2 y-1)
3 0.24 2004 0.9 0.27
6 0.31 2003 1.8 0.17
9 0.36 2002 2.9 0.12
12 0.42 2001 4.2 0.10 Monthly water monitoring program (since 1997),
Water hyacinth proliferation (1994–1998),
Plant removal and beginning of hypertrophic phase
(1999)
18 0.48 1996 9.3 0.05
26 0.45 1991 13.8 0.03 Erosion of lake margin
34 0.32 1985 20.4 0.02
38 0.35 1980 24.8 0.01
41 0.36 1977 27.8 0.01
43 0.36 1975 30.1 0.01 Installation of Sao Paulo State Department of
Agriculture (deforestation and sewage loadings)
45 0.86 1971 34.4 0.02
48 0.85 1962 43.3 0.02
49 0.96 1958 47.1 0.02 City zoo construction (increased sewage loadings)
51 1.12 1951 53.8 0.02
56 1.38 1928 76.7 0.02 Initial establishment of public buildings
57 1.40 1923 81.8 0.02
58 1.35 1919 86.1 0.02 Division of the previous water supply reservoir into five
water bodies (*1917)
756 J Paleolimnol (2012) 48:751–766
123
and very fine sand (63 lm). Notable exceptions were
the 55 cm (*1932) layer that was composed of
medium sand (250 lm), 54 cm (*1938), composed
of fine sand (125 lm), and the 52 cm (*1947) and
22 cm (*1993) samples, which were composed of
very fine sand (63 lm) (Fig. 3).
Geochemistry
The TOC and TN profiles exhibit parallel changes
(Fig. 4). TOC was low (1.0 %) until 50 cm (*1955),
and increased steadily, reaching a maximum (9.5 %)
in the upper part of the core (1–3 cm, *2005). TN
values were below the detection limit (0.01 % or
100 lg N g-1 dw) at around 61 cm (*1907), and
gradually increased, reaching a maximum at the core
surface (1.35 %). The C/N ratio varied from 7 to 21,
decreasing towards the core top, with values below 10
above 24 cm (*1993) (Fig. 4). TP concentrations
varied from 0.03 to 0.58 %, and showed a consistent
increase since *1975, and mainly since *1991
(26 cm) towards the top of the core (Fig. 4). The
marked increase in TN since *2000 is consistent with
the monitoring data, and was probably associated with
the twofold increase in TN loadings, whereas P input
was unchanged during this period (Table 1).
Diatom assemblages
A total of 80 diatom species were identified in the core,
but only those with abundances C5 % in at least one
sample are plotted in Fig. 5 (22 taxa). Cluster analysis
identified four major diatom assemblage zones (DAZ)
and two subzones. Diatoms were either absent or were
poorly preserved prior to *1919 (58 cm).
DAZ 1a (58–53 cm; ca. 1919 to 1943)—This
subzone was dominated by A. granulata (Ehr.)
Simonsen var. granulata (up to 54.5 %). Fragilaria
capucina Desmazieres occurred in almost the entire
zone, with low to moderate abundances (8–24 %), and
D. stelligera (Cleve & Grun.) Houk & Klee (21 %),
Aulacoseira ambigua (Grunow) Simonsen (19 %) and
Achnanthidium catenatum (Bily & Marvan) Lange-
Bertalot (13 %) were also relatively abundant.
DAZ 1b (53–43 cm; ca. 1944–1975) was charac-
terized by high species richness (species number per
sample). Diadesmis contenta (Grunow ex V. Heurck)
Mann was the most abundant taxon (37–50 %), and
several other taxa that were observed in DAZ 1a were
also present in relatively high abundances (Luticola
mutica (Hustedt) Mann, Frustulia crassinervia (Breb.)
Lange-Bertalot & Krammer, Nitzschia terrestris (Pet-
ersen) Hustedt, Eunotia rabenhorsti Cleve & Grunow,
and Brachysira brebissonii Ross in Hartley). Six new
species appeared in this zone (Brachysira vitrea
(Grunow) Ross in Hartley, Eunotia quaternaria Ehr.,
Encyonopsis microcephala (Grunow) Krammer, Han-
tzschia amphioxys (Ehr.) Grunow, Planothidium ro-
stratum (Oestrup) Lange-Bertalot and Pinnularia
dubitabilis (Hustedt) Hustedt). Aulacoseira granulata
var. granulata sharply decreased.
Fig. 3 Grain size composition of the LG05-03 core
J Paleolimnol (2012) 48:751–766 757
123
DAZ 2 (43–30 cm; ca.1976–1988)—species rich-
ness abruptly declined at the DAZ1b/2 boundary with
many of the taxa that appeared in DAZ1b disappearing
from the record. Discostella stelligera dominated
DAZ 2 (up to 92 %), but sharply decreased towards
the top of this zone. Three other taxa, F. capucina,
A. ambigua and A. granulata var. granulata were also
present in relatively high abundances.
DAZ 3 (30–22 cm; ca. 1989–1994)—A. catenatum
(Bily & Marvan) Lange-Bertalot was dominant in this
zone (up to 77 %). The four most abundant taxa in
DAZ 2 decreased appreciably in their abundances
(F. capucina, D. stelligera, A. granulata var. granu-
lata, and A. ambigua).
DAZ 4a (22–14 cm; ca.1995–1999)—A. catena-
tum declined markedly, but remained the most abun-
dant species (36 %). Another notable feature was the
expansion of P. rostratum (Oestrup) Lange-Bertalot
(26 %) and C. meneghiniana (12 %).
DAZ 4b (14–0 cm; ca. 2000–2005)—this zone
saw the further expansion of P. rostratum (up to 51 %)
and C. meneghiniana (48 %), whereas A. catenatum
remained an important component of the assemblage
(30 %). In contrast, F. capucina and D. stelligera
decreased to negligible relative abundances (1 %).
Principal component analysis
According to the broken-stick model, PCA extracted
two interpretable axes of variation in the diatom
relative abundance data (43 species with abundances
C1 %) accounting for 40 % of the total variation
(Fig. 6). Samples were clearly separated over time.
Samples from DAZ 1b (ca. 1944–1975) were
Fig. 4 Down-core variations in % total phosphorus (TP), total nitrogen (TN), total organic matter and C/N ratio values for the LG05-3
core
758 J Paleolimnol (2012) 48:751–766
123
positioned on the left of the diagram associated with
negative Axis 1 scores, and samples from DAZ 2–4
were located on the right of the plot with positive Axis
1 scores. DAZ 1a, which grouped with DAZ 2,
apparently was an exception, as explained below.
Seventeen species showed high correlation
(r C 0.5) with the negative side of Axis 1, and
therefore, with the period prior to *1975. The species
(ordered by decreasing correlation) are: D. contenta
(DCON), B. brebissonii (BBRE), L. mutica (LMUT),
N. terrestris (NTER), F. crassinervia (FCRA), L. mu-
ticoides (LMUC), Pinnularia sp. (PINN), E. raben-
horstii (ERAB), E. sudetica (ESUD), P. dubitabilis
(PDUB), P. subcapitata (PSUB), Gomphonema parv-
ulum (GPAR), Rhopalodia sp.1 (RHOP), E. micro-
cephala (EMIC), Eunotia tenella (ETEN) and
Luticola goeppertiana (LGOP). Conversely, seven
species had high correlation (r C 0.5) with the
positive side of Axis 1, i.e. mostly after 1975, namely
(in order of decreasing correlation) C. meneghiniana
(CMEN), A. catenatum (ADCT), F. capucina (FCAP),
A. minutissimum (ADMI), A. granulata var. granulata
(AUGR), A. granulata var. angustissima (AUGA) and
Ulnaria ulna (UULN). On Axis 2, samples from the
DAZ 2 period (ca. 1976–1988) were separated from
those of DAZ 3 and 4 (ca.1989–2005). Two species,
D. stelligera (DSTE) and A. ambigua (AAMB),
exhibited high association with DAZ 2 whereas
P. rostratum (PLRO), Achnanthidium exiguum var.
exiguum (ADEG), C. meneghiniana (CMEN) and
A. catenatum (ADCT) were associated with DAZ 4
and to a lesser extent with DAZ 3 (ca. 2000–2005).
DAZ 1a samples were grouped with DAZ 2 as a
consequence of the dominance of A. granulata var.
granulata (AUGR) at the core base. The PCA showed
that the diatom assemblages underwent a sharp change
after *1975, followed by a second large shift in
*1990.
Discussion
The main changes in lithology, grain size and geo-
chemistry, as well as in the key events recorded by
land use history (Table 2) and monitoring data, were
in agreement with the four major diatom assemblage
zones. These zones were also highlighted by PCA
analysis, which clearly separated the zones along the
main axes of variation (Fig. 6). The interpretation of
diatom zones starts after *1919 (58 cm) because
Fig. 5 Summary of the diatom assemblages (species abundances C5 %) from Garcas Reservoir core LG05-04, (horizontal linesdenote the zones identified by CONISS)
J Paleolimnol (2012) 48:751–766 759
123
valves were absent or poorly preserved prior to this
time. This period is likely to represent the creek phase,
the period of the dam construction, which started in
1894 and the physical alterations of the water supply
reservoir since *1917 (according to state government
records). This assumption was supported by the sand
composition of the core base (Fig. 3), indicating a
period of higher water flux and energy (Abraham et al.
1999). Furthermore, the simultaneous increase of TN
content since *1912, along with the high C/N ratio
(21) suggests the reservoir creation phase, associated
with vegetation flooding, given that C/N atomic ratios
above 20 are typically related to the prevalence of
organic matter derived from vascular plants (Meyers
2003). Therefore, the diatom record represents the
reservoir history since *1920, and was separated into
six main periods that are described below.
DAZ 1a—high physical/hydrological anthropo-
genic impact, minor anthropogenic eutrophication;
initial establishment of public buildings in the catch-
ment, former water supply reservoir phase—ca.
1919–1943 (DAZ 1a, 58–53 cm):
The present Garcas Reservoir originated during the
period represented by DAZ 1a, by division of the
previous water supply reservoir into five water bodies
since *1917. From *1919 to *1931, the sediments
were mainly composed of coarse silt to very coarse silt
(Fig. 3), indicating the start of the Garcas Reservoir,
and the associated physical/hydrological changes.
Grain size data reveal a switch to medium sand in
*1932 and fine sand in *1938, coinciding with the
initial establishment of public buildings in the PEFI
and the opening of the Sao Paulo State Botanical
Garden. In *1928, water provision ceased as a
consequence of the continued increase in the local
population, risk of water pollution, and the intention of
the Sao Paulo State government to establish public
institutions and parks in the area (Rocha and Caval-
heiro 2001).
Phosphorus concentrations remained relatively
low, whereas nitrogen and carbon increased slightly
during this period. C/N ratios decreased to 13, but still
indicate the prevalence of a vascular organic matter
source to the system (Meyers 2003).
Fig. 6 PCA biplot of sample and species scores from Garcas
Reservoir core LG05-04 based on diatom taxa with abundances
C1 %. See text for species abbreviations. Samples are classified
by diatom assemblage zones: DAZ 1a, DAZ 1b, DAZ 2, DAZ 3,
DAZ 4a and DAZ 4b. Vectors with correlations below 0.3 are
not shown
760 J Paleolimnol (2012) 48:751–766
123
Several diatom species were present in low abun-
dances in DAZ 1a (B. brebissonii, E. rabenhorstii,
L. mutica, F. crassinervia, N. terrestris, E. sudetica
and D. contenta), suggesting an oligotrophic system at
that time. These species are mainly aerophilic and
most are considered acidophilic, with high oxygen
requirements (van Dam et al. 1994; Hoffman 1994;
Battarbee et al. 2001b; http://craticula.ncl.ac.uk/Eddi/
jsp/), and are typically associated with low nutrient
availability (van Dam et al. 1994; Poulıckova et al.
2004; Poulıckova and Hasle 2007).
Discostella stelligera, a relatively abundant species
in this subzone, probably reflects deforestation events
that occurred to make way for building construction
(1928, 1932) and the opening of streets (1938) in the
reservoir catchment (according to state government
records). The change in land use in the catchment was
also indicated by the change in grain size, from silt to
fine sand, and the increasing organic carbon content.
This inference is in accordance with Koster et al.
(2005) who observed the increasing abundance of
D. stelligera with the first anthropogenic disturbances
caused by timber harvesting, reflecting the removal of
vegetation in the Walden Pond watershed.
Aulacoseira granulata dominates this subzone.
This species has been typically reported in eutrophic
waters (Zalat 2000; Stoof-Leichsenring et al. 2011), as
well as in highly productive and oligotrophic lakes in
Chile (Cruces et al. 2001), and as dominant in
subtropical shallow lakes with low TP concentration
(Yang et al. 2008). In our study this species was not
considered a good indicator of trophic status, because
it also prevailed in DAZ 2 when nutrient concentra-
tions were much higher. Indeed, this species has been
associated with physical alterations such as depth
variation, turbulence and mixing regime (Zalat 2000;
Caballero et al. 2006; Dong et al. 2008). Therefore, the
predominance of planktonic taxa in DAZ 1a, princi-
pally A. granulata and D. stelligera, most likely
indicates the phase of high physical alteration associ-
ated with deforestation and the initial establishment of
public buildings, leading to higher water turbulence
and a decrease in light availability.
DAZ 1b—Minor hydrological/physical anthropo-
genic impact, moderate eutrophication impact, city zoo
construction—ca. 1944–1975 (DAZ 1b, 53–43 cm):
In 1958 the city zoo was established (covering an
area of 830,000 m2) in the PEFI area and untreated
effluent began to discharge to the reservoir. This
period was characterized by the gradual increase in
geochemical proxies for trophic state (TP, TN, TOC)
along with a decrease in C/N ratios to 11, although
values still indicate the prevalence of a vascular plant
source to the system (Meyers 2003).
This period was characterized by the highest diatom
species richness (species number per sample) and the
prevalence of benthic taxa, namely D. contenta,
L. mutica, F. crassinervia, N. terrestris and E.
rabenhorstii. These are aerophilic and indicators of
low-nutrient environments (van Dam et al. 1994;
Poulıckova et al. 2004; http://craticula.ncl.ac.uk/Eddi/
jsp/).
A clear shift from planktonic (D. stelligera,
A. ambigua and A. granulata) to benthic species
occurred in this subzone. This habitat shift could result
from the sharp reduction of the reservoir area in DAZ
1a, followed by a period of minor physical alterations.
These changes supposedly promoted a decrease in
water turbulence and turbidity, an increase in light
regime and the broadening of littoral areas, leading to
benthic habitat expansion. The end of this zone
(*1975) was highlighted by PCA (Fig. 6) as marking
the onset of the limnological changes that were a
consequence of anthropogenic eutrophication.
DAZ 2—high physical anthropogenic impact,
moderate to high anthropogenic eutrophication, Sao
Paulo State Department of Agriculture and Provision-
ing headquarters construction, first signs of eutrophi-
cation—ca. 1976–1988 (DAZ 2, 43–30 cm):
This period marks the establishment of the Sao
Paulo State Department of Agriculture and Provision-
ing headquarters (*80,000 m2) in 1975, the associ-
ated major deforestation and erosion events, and the
additional untreated sewage input to Garcas Reservoir.
Geochemical proxies for trophic state, mainly TP,
continue to increase in DAZ 2 (Fig. 4). The sediments,
composed of fluid black mud, indicate higher levels of
organic matter, and the C/N ratios (11–12) suggest the
continued prevalence of vascular plant productivity
(Meyers 2003). However, the decline in the sediment
TN/TP ratio from 2.4 (DAZ 1b) to 1.6 (DAZ 2) reflects
higher phosphorus input in this zone.
Species richness declined, and the diatom assem-
blages became dominated by planktonic taxa with
almost complete replacement of benthic species
(Fig. 5). This assemblage shift suggests a deteriorating
light climate for macrophytes and attached forms. In
this respect, the dominance of D. stelligera (91–92 %)
J Paleolimnol (2012) 48:751–766 761
123
*1977–1978 is most likely associated with the
deforestation required for the construction of the
Department of Agriculture buildings. Increased abun-
dance of D. stelligera, associated with vegetation
removal, has been reported in other studies (Fritz et al.
1993; Lotter 2001; Koster et al. 2005). Furthermore,
the expansion of F. capucina, A. ambigua and A. gran-
ulata observed in this zone is consistent with physical
alterations, particularly to light conditions, as a con-
sequence of deforestation, erosion, silt inwash, and
turbulence, as reported elsewhere (Velez et al. 2003;
Koster and Pienitz 2006; Yang et al. 2008). In terms of
trophic status, D. stelligera has been associated with an
increase in P availability (Baier et al. 2004; Koster and
Pienitz 2006), F. capucina has been reported in low to
moderately nutrient-rich waters (http://craticula.ncl.
ac.uk/Eddi/jsp/), A. ambigua in mesotrophic to eutro-
phic environments (Caballero et al. 2006), and A.
granulata in both highly productive and oligotrophic
lakes (Cruces et al. 2001; Yang et al. 2008; Stoof-
Leichsenring et al. 2011). In Garcas Reservoir, the
above species appear more likely to be associated with
physical alterations (deforestation, erosion, light cli-
mate) than to the increasing P inputs, especially as
these same species were also found in DAZ 1a (Fig. 5),
when the reservoir was relatively nutrient-poor.
At this time in the reservoir history, prevalence of
benthic diatom species in DAZ 1b, and to a lesser
extent in DAZ 2, indicates continued habitat avail-
ability for macrophytes. Given that submerged mac-
rophytes play an important role in shallow lakes
resisting increased limnetic nutrient concentrations
(Scheffer et al. 1993), loadings were probably still too
low to push the reservoir into a eutrophic state.
DAZ 3—High anthropogenic impact; onset of
marked eutrophication—ca. 1989–1994 (DAZ 3,
30–22 cm):
This zone was characterized by an abrupt increase
in TP content (15-fold higher than values at the core
base), clearly related to the increasing sewage loadings
from the zoo and the Sao Paulo State Department of
Agriculture. C/N ratios declined to 10, indicating a rise
in autochthonous productivity (Meyers 2003), and
TN/TP decreased from 1.6 (DAZ 2) to 1.3, reflecting
the relative higher P inputs.
Discostella stelligera abundance decreased mark-
edly from 22 % (*1990) to 2 % (*1991), possibly
associated with the elevated productivity of the lake.
Similarly, a rise in D. stelligera with deforestation,
followed by its decline with further nutrient enrich-
ment, was reported by Koster et al. (2005).
At the beginning of this zone, a marked increase
in Aulacoseira alpigena was observed, immediately
followed by dominance of A. catenatum (77 %) in
*1993. The former species was reported as a typical
indicator of eutrophication in a diatom-TP data set for
Chinese lakes (Yang et al. 2008). However, ecological
information for A. catenatum is very scarce (Straub
2002), perhaps as a consequence of its common
misidentification as A. minutissimum, as well as its
tropical origin (Coste and Ector 2000). This species has
a colonial life form that differs from all other Achnan-
thidium species, and has been reported as planktonic
(Hlubikova et al. 2011). It has been considered an
invasive tropical species in different parts of Europe,
and is also reported as a bloom-forming species,
probably associated with warming climate (Coste and
Ector 2000; Straub 2002). This fast-growing species is
possibly favored by higher temperature, although in
tropical lakes it seems to be more associated with
eutrophication. Achnanthidium catenatum has been
reported in mesotrophic environments (Hoffman 1994),
and is well represented in mesotrophic to eutrophic
conditions (Lange-Bertalot and Steindorf 1996). In our
study, this species peaked when P levels abruptly
increased and P loadings were higher in relation to TN
inputs. This opportunistic species is probably indicative
of a critical limnological alteration, such as the shift
from a mesotrophic to eutrophic state.
The major compositional shifts in this zone were
clearly captured by PCA (Fig. 6), indicating major
ecological change in the reservoir from the early
1990s. Planktonic opportunistic species that compete
well in eutrophic waters prevailed in DAZ 3, suggest-
ing the onset of a marked eutrophication phase and the
change from clear to turbid waters.
DAZ 4a—Very high anthropogenic impact; major
eutrophication phase—ca. 1995–1999 (DAZ 4a,
22–14 cm):
The water-monitoring program started in 1997
(Table 1) and the reservoir was classified as eutrophic,
with cyanobacteria blooms during spring (Bicudo
et al. 2007). According to Bicudo et al. (2007), the
reservoir underwent a striking limnological change as
a consequence of a water hyacinth outbreak (May
1998–September 1999) that covered 40–70 % of the
reservoir surface area, followed by almost complete
plant removal at the end of this zone.
762 J Paleolimnol (2012) 48:751–766
123
The planktonic diatom component clearly declined
in abundance (Fig. 5). The physical changes brought
about by hyacinth proliferation, such as decreased light
availability and additional surfaces for epiphyton
growth, probably explain the rapid decrease in the
planktonic taxon A. catenatum and the concomitant
increase in P. rostratum, a species typically observed in
the epiphyton of eutrophic systems (Pan and Brugam
1997; van Dam et al. 1994; http://craticula.ncl.ac.uk/
Eddi/jsp/). According to King et al. (2006), this species
can survive for long periods ([30 days) in a heterotro-
phic state, giving it a competitive advantage over other
species, especially under low light conditions, such as
under the water hyacinth canopy of the Garcas
Reservoir.
In this zone, the epilimnetic nutrient concentra-
tions, particularly TP, were probably buffered by
macrophytes, despite the increasing loadings to the
system (Table 1). Nutrient storage by water hyacinth
has been well documented (Rommens et al. 2003).
However, at the end of DAZ 4a, the mechanical
removal of water hyacinth (3,100 m3) over a period of
three months triggered the shift of Garcas Reservoir to
a stable, degraded state with hypereutrophic nutrient
concentrations and permanent cyanobacterial blooms
(Bicudo et al. 2007). Since the end of 1999, only 10 %
of the original plant cover has been retained by wire
screens placed near the zoo outflows.
DAZ 4b—Very high anthropogenic impact; hyper-
trophic phase—2000–2005 (DAZ 4b, 14–0 cm):
This zone marks a highly degraded phase for Garcas
Reservoir. The plant removal modified nutrient dynam-
ics, reduced oxygen content of the bottom water, and led
to an increase in cyanobacteria biomass which became an
effective barrier to light penetration (Bicudo et al. 2007).
Monitoring data revealed a notable increase in TN
loading from the period represented by DAZ 4a
(1997–1999) to that of DAZ 4b (2000–2004). Whereas
TP input remained similar, epilimnetic TP and bottom-
water soluble reactive phosphorus concentrations mark-
edly increased, suggesting the occurrence of internal P
loading (Bicudo et al. 2007, Table 1).
Steady increases in nutrient concentrations were
tracked by geochemical variables TP, TN, TOC, with
highest values at the core top. In contrast, C/N ratios
were at their lowest (7), pointing to the prevalence of a
nitrogen-rich, proteinaceous organic matter source such
as phytoplankton (Meyers 2003). The data are consistent
with the hypereutrophic state of the reservoir.
Although it is reasonable to consider that nutrients
are a key force behind the diatom assemblage shifts in
DAZ 4b, there are other important interacting factors
to consider, such as light regime, pH changes
(Table 1), and shifts in the dominance of different
cyanobacteria functional groups.
The replacement of A. catenatum by P. rostratum
intensified in this zone until *2002, when the latter
reached its highest abundance (Fig. 5). During this
period, Microcystis species dominated the phyto-
plankton (80–90 % of total biovolume), increasing
light limitation and creating a highly selective envi-
ronment (Crosseti and Bicudo 2008), which probably
impaired A. catenatum growth. Conversely, P. rostra-
tum has a selective advantage under low irradiance
conditions (King et al. 2006), and is considered an
alkaliphilous species, occurring mainly at pH [ 7
(Cox 1996). Thus the conditions following plant
removal (Table 1) most likely favored P. rostratum.
This species is typically observed in the epiphyton of
eutrophic systems (Pan and Brugam 1997), so the
valves accumulated in the sediments probably origi-
nated from the water hyacinth stand maintained in the
reservoir and other available surfaces.
Cyclotella meneghiniana steadily increased after
the peak of P. rostratum, reaching dominance towards
the core top (Fig. 5). This period was characterized by
the replacement of M. aeruginosa by C. raciborskii
blooms, higher transparency, reduction of the water
column stability and of the bottom water SRP content
(Crosseti and Bicudo 2008). During 2006–2007,
Ferrari (2010) reported that higher N availability
(high N/P ratios), reduction of the thermal stability and
of the bloom biomass (M. aeruginosa) favored C.
meneghiniana growth in Garcas Reservoir. Indeed,
these conditions, including higher geochemical TN/
TP ratios (1.9–2.5), occurred at the end of DAZ 4b.
Cyclotella meneghiniana has been widely studied and
shown to be tolerant of elevated pollution levels,
occurring in lakes that receive urban and industrial
wastewater (Sabater and Sabater 1988; van Dam et al.
1994), and has been reported as dominant in hypereu-
trophic Chinese lakes (Yang et al. 2008).
Conclusions
Reconstruction of anthropogenic impacts in the Gar-
cas Reservoir, SE Brazil, over the last 110 years
J Paleolimnol (2012) 48:751–766 763
123
(1894–2005) revealed that eutrophication was a key
driver of chemical and biological changes. Diatom
assemblage shifts, however, responded to multiple
stressors and our data highlight the interplay between
anthropogenically induced hydrological/physical
changes and eutrophication.
Multi-proxy analysis of the sediment record, cou-
pled with the land-use history, provides a comprehen-
sive approach to tracking lake response to multiple
stressors, and provides information on the likely
causes of the observed ecological changes. Further-
more, land-use history, grain size changes and water
quality monitoring data proved valuable for validating
the sediment chronology.
The main shifts between planktonic and benthic
diatom assemblages appear to track major limnolog-
ical changes associated with complex interactions
among physical, hydrological factors and eutrophica-
tion: (1) first, prevalence of benthic over planktonic
species resulted from the sharp reduction of the
reservoir area (since DAZ 1a), along with a period
of minor physical alterations (DAZ 1b), (2) second,
the major shift to planktonic species dominance (from
DAZ 1b to DAZ 2) was most likely associated with
deforestation and erosion events that were a conse-
quence of the establishment of the Sao Paulo State
Department of Agriculture Headquarters, (3) third,
marked expansion of A. catenatum indicated the onset
of the eutrophication phase, and (4) fourth, dominance
of P. rostratum and C. meneghiniana suggested a shift
to a hypereutrophic state, since 1999, as a result of
increased external and internal nutrient loading.
In summary, our results show that sedimentary
diatom assemblages, supported by other sediment
variables, are effective for tracking ecological shifts in
tropical reservoir ecosystems. Additionally, our data
highlight the great importance of hydrological/phys-
ical changes as drivers of diatom assemblage changes
in reservoirs relative to natural systems. Thus, inter-
pretation of planktonic/benthic shifts in reservoir
contexts must not be assumed to have been driven
solely by eutrophication.
Finally, this study highlights the need for greater
autoecological information and the development of
quantitative approaches such as diatom transfer func-
tions for tropical lakes and reservoirs in Brazil. Such
information would improve interpretation of sedimen-
tary diatom records and enhance their value for
managers and conservationists.
Acknowledgments This work was supported by funds
provided by Fundacao de Amparo a Pesquisa do Estado de Sao
Paulo (FAPESP), and was undertaken as part of a PhD thesis
(FAPESP doctoral fellowship 04/08675-8 to SCB) at the
Instituto de Botanica (Sao Paulo, Brazil). Funds were also
provided by Conselho Nacional de Desenvolvimento Cientıfico
e Tecnologico (CNPq) (Grants 472035/2006-1 and 305072/
2009-9 to DCB). We deeply appreciate the valuable assistance of
Prof. Dr. Paulo de Oliveira and the Jabaquara Fireman
Corporation with the core sampling. We are grateful to Prof.
Dr. Antonio A. Mozeto for the laboratory facilities for
geochronology analyses, and to Prof. Dr. Marcio Roberto
Magalhaes de Andrade and Prof. Esp. William de Queiroz for
providing the illustration of the study area. We also thank all the
students and technicians involved in the laboratory and
fieldwork. We appreciate the two journal reviewers and the
editors, for providing helpful comments that improved the
quality of the manuscript.
References
Abraham J, Allen PM, Dunbar JA, Dworkin SI (1999) Sediment
type distribution in reservoirs: sediment source versus
morphometry. Environ Geol 38:101–110
Andersen JM (1976) An ignition method for determination of
total phosphorus in lake sediments. Water Res 10:329–331
Appleby PG, Oldfield F (1978) The calculation of Pb-210 dates
assuming a constant rate of supply of unsupported Pb-210
to the sediment. Catena 5:1–8
Baier J, Lucke A, Negendank JFW, Schleser GH, Zolitschka B
(2004) Diatom and geochemical evidence of mid-to late
Holocene climatic changes at Lake Holzmaar, West Eifel
(Germany). Quat Int 113:81–96
Battarbee RW, Jones VJ, Flower RJ, Cameron NG, Bennion H,
Carvalho L, Juggins S (2001a) Diatoms. In: Smol JP, Birks
HJB, Last WM (eds) Tracking environmental change using
lake sediments. vol 3: terrestrial, algal, and siliceous indi-
cators. Kluwer, Dordrecht, pp 155–202
Battarbee RW, Juggins S, Gasse F, Anderson NJ, Bennion H,
Cameron NG, Ryves DB, Pailles C, Chalie F, Telford R
(2001b) European diatom database (EDDI). An informa-
tion system for palaeoenvironmental reconstruction.
ECRC Research Report No 81, University College Lon-
don, 94 pp
Battarbee RW, Anderson NJ, Jeppensen E, Leavitt PR (2005)
Combining paleolimnological and limnological approa-
ches in assessing lake ecosystem response to nutrient
reduction. Freshw Biol 50:1772–1780
Bennion H, Battarbee RW (2007) The European union water
framework directive: opportunities for palaeolimnology.
J Paleolimnol 38:285–295
Bennion H, Fluin J, Simpson GL (2004) Assessing eutrophica-
tion and reference conditions for Scottish freshwater lochs
using subfossil diatoms. J Appl Ecol 41:124–138
Bennion H, Battarbee RW, Sayer CD, Simpson GL, Davidson
TA (2011) Defining reference conditions and restoration
targets for lake ecosystems using palaeolimnology: a syn-
thesis. J Paleolimnol 45:533–544
764 J Paleolimnol (2012) 48:751–766
123
Bicudo DC, Fonseca BM, Bini LM, Crossetti LO, Bicudo CEM,
Araujo-Jesus T (2007) Undesirable side-effects of water
hyacinth control in a shallow tropical reservoir. Freshw
Biol 52:1120–1133
Blott SJ, Pye K (2001) Gradistat: a grain size distribution and
statistics package for the analysis of unconsolidated sedi-
ments. Earth Surf Process Landforms 26:1237–1248
Caballero M, Vasquez G, Lozano-Garcıa S, Rodrıguez A, Sosa-
Najera S, Ruiz-Fernandez AC, Ortega B (2006) Present
limnological conditions and recent (ca. 340 yr) paleo-
limnogical of a tropical lake in the Sierra de Los Tuxtlas,
eastern Mexico. J Paleolimnol 35:83–97
Cazotti RI, Gomes ACF, Nascimento MRL, Mozeto AA (2006)
Geocronologia isotopica (210Pb e 226Ra) de sedimentos
lımnicos: determinacao de velocidades e taxas de sedi-
mentacao e de idades. In: Mozeto AA, Umbuzeiro GA,
Jardim WF (eds) Metodos de coleta, analises fisico-quım-
icas e ensaios biologicos e ecotoxicologicos de sedimentos
de agua doce. Cubo Editora, Sao Carlos, pp 37–39 (Isotopic
geochronology - 210Pb and 226Ra -of lake sediments: cal-
culation of sediment accumulation rates and ages.)
Coste M, Ector L (2000) Diatomees invasives exotiques ou rares
em France: principales observations effectuees au cours
des dernieres decennies. Syst Geogr Plants 70:373–400
(Invasive, exotic or rare diatoms in France: main obser-
vations during the last decades)
Cox EJ (1996) Identification of freshwater diatoms from live
material. Chapman & Hall, London, p 158
Crosseti L, Bicudo CEM (2008) Phytoplankton as a monitoring
tool in a tropical urban shallow reservoir (Garcas Pond):
the assemblage index application. Hydrobiol 610:161–173
Crossetti LO, Bicudo DC, Bicudo CEM, Bini LM (2008) Phyto-
plankton biodiversity changes of a shallow tropical reservoir
during the hypertrophication process. Braz J Biol 68:631–637
Cruces F, Urrutia R, Araneda A, Torres L, Cisternas M, Vyv-
erman W (2001) Evolucion trofica de Laguna Grande de
San Pedro (VIII region, Chile) durante el ultimo siglo,
mediante el analisis de registros sedimentarios. Rev Chil
His Nat 74:407–418 (Trophic Evolution of Laguna Grande
de San Pedro (VIII Region, Chile) during the last century,
by means of the analysis of sedimentary records)
Dixit AS, Alpay S, Dixit SS, Smol JP (2007) Paleolimnological
reconstructions of Rouyn-Noranda lakes within the zone of
influence of the Horne Smelter, Quebec, Canada. J Paleo-
limnol 38:209–226
Dong X, Bennion H, Battarbee RW, Yang X, Yang H, Liu E (2008)
Tracking eutrophication in Taihu Lake using the diatom
record: potential and problems. J Paleolimnol 40(1):413–429
Ferrari F (2010) Estrutura e dinamica da comunidade de algas
planctonicas e perifıticas (com enfase nas diatomaceas) em
reservatorios oligotrofico e hipertrofico (Parque Estadual
das Fontes do Ipiranga, Sao Paulo). Rio Claro: UNESP,
PhD thesis. 343p (Periphytic and phytoplanktonic com-
munity structure (with emphasis on the diatoms) in oligo-
trophic and hypertrophic reservoirs)
Findlay DL, Kling HJ, Ronicke H, Findlay WJ (1998) A pa-
leolimnological study of eutrophied Lake Arendsee (Ger-
many). J Paleolimnol 19:41–54
Fritz SC, Kingston JC, Engstrom DR (1993) Quantitative tro-
phic reconstruction from sedimentary diatom assemblages:
a cautionary tale. Freshw Biol 30:1–23
Grimm EC (1991) TILIA version 1.11. TILIAGRAPH version
1.18. In: Gear A (ed) A users notebook. Illinois State
Museum, Springfield, USA
Hall RI, Smol JP (2010) Diatoms as indicators of eutrophication.
In: Smol JP, Stoermer EF (eds) The diatoms: applications
for the environmental and earth sciences, 2nd edn. Cam-
bridge University Press, Cambridge, pp 122–151
Hedges JI, Stern JH (1984) Carbon and nitrogen determinations of
carbonate-containing solids. Limnol Oceanogr 29:657–663
Hlubikova D, Ector L, Hoffmann L (2011) Examination of the
type material of some diatom species related to Achnan-thidium minutissimum (Kutz.) Czarn. (Bacillariophyceae).Algol Stud 136(137):19–43
Hoffman G (1994) Aufwuch-Diatomees in Seen und ihre Eig-
nung als Indikatoren der Trophie. Bibl Diatomol 30:241
(Periphytic diatoms in lakes and their application as trophic
indicators)
Jackson DA (1993) Stopping rules in principal component
analysis: a comparison of heuristical and statistical
approaches. Ecology 74:2204–2214
Johnes PJ (1999) Understanding lake and catchment history as a
tool for integrated lake management. Hydrobiologia
395(396):41–60
Juggins S (2003) C2 user guide. Software for ecological and
palaeoecological data analysis and visualisation. Univer-
sity of Newcastle, Newcastle upon Tyne 69 p
Juttner I, Chimonides PJ, Ormerod SJ (2010) Using diatoms as
quality indicators for a newly-formed urban lake and its
catchment. Environ Monit Assess 162:47–65
King L, Clarke G, Bennion H, Kelly M, Yallop M (2006)
Recommendations for sampling littoral diatoms in lakes
for ecological status assessments. J Appl Phycol 18:15–25
Kirilova EP, van Hardenbroek M, Heiri O, Cremer H, Lotter AF
(2010) 500 years of trophic-state history of a hypertrophic
Dutch dike-breach lake. J Paleolimnol 43:829–842
Koster D, Pienitz R (2006) Seasonal diatom variability and
paleolimnological inferences—a case study. J Paleolimnol
35:395–416
Koster D, Pienitz R, Wolfe BB, Barry S, Foster DR, Dixit SS
(2005) Paleolimnological assessment of human-induced
impacts on Walden Pond (Massachusetts, USA) using
diatoms and stable isotopes. Aquat Ecosyst Health Manag
8:117–131
Lange-Bertalot H, Steindorf A (1996) Rote Liste der limnisch-
hen Kieselalgen (Bacillariophyceae) Deutschlands. Sch-
riftenr Vegetationskunde 28:633–677 (Red list of
freshwater diatoms (Bacillariophyceae) in Deustchland)
Lewis WM (2000) Basis for the protection and management of
tropical lakes. Lake Reservoir Manag 5:35–48
Liu J, Zhang H, Han B (2012) Hydrodynamic change recorded
by diatoms in sediments of Liuxihe Reservoir, southern
China. J Paleolimnol 47:17–27
Lotter AF (2001) The palaeolimnology of Soppensee (Central
Switzerland) as evidenced by diatom, pollen and fossil –
pigment analyses. J Paleolimnol 25:65–79
McCune BMJ, Mefford MJ (1999) PC-ORD Multivariate
analysis of ecological data. Version 4.10. MJM. Software
design, Oregon, p 47
Metzeltin D, Lange-Bertalot H (2007) Tropical diatoms of
South America, 2. In: Lange-Bertalot H (ed) Iconographia
J Paleolimnol (2012) 48:751–766 765
123
diatomologica, annotated diatom micrographs, vol 15.
Koeltz Scientific Books, Sttutgart, p 736
Metzeltin D, Lange-Bertalot H, Garcia-Rodriguez F (2005)
Diatoms of uruguay. Iconogr Diatomol 15:1–736
Meyers PA (2003) Applications of organic geochemistry to
paleolimnological reconstructions: a summary of examples
from the Laurentian Great Lakes. Org Geochem 34:
261–289
Pan Y, Brugam R (1997) Human disturbances and trophic status
changes in Crystal Lake, McHenry County, Illinois, USA.
J Paleolimnol 17:369–376
Poulıckova A, Hasle P (2007) Aerophytic diatoms from caves in
central Moravia (Czech Republic). Preslia 79:185–204
Poulıckova A, Hajkova P, Krenkova P, Hajek M (2004) Dis-
tribution of diatoms and bryophytes on linear transects
through spring fens. Nova Hedwigia 78:411–424
Rocha YT, Cavalheiro F (2001) Aspectos historicos do Jardim
Botanico de Sao Paulo. Rev Brasil Bot 24:577–586 (His-
torical aspects of the Botanical Garden of Sao Paulo)
Rommens W, Maes J, Dekeza N, Inghelbrecht P, Nhiwatiwa T,
Holsters E, Ollevier F, Marshall B, Brendonck L (2003)
The impact of water hyacinth (Eichhornia crassipes) in a
eutrophic subtropical impoundment (Lake Chivero, Zim-
babwe), 1: water quality. Archiv fur Hydrobiologie 158:
373–388
Sabater S, Sabater F (1988) Diatom assemblages in the River
Ter. Arch Hydrobiol 111:397–408
Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993)
Alternative equilibria in shallow lakes. Trends Ecol Evol
8:275–279
Smol JP (2008) Pollution of Lakes and Rivers—a paleoenvi-
ronmental perspective, 2nd edn. Blackwell Publishing,
Oxford 383 pp
Stoof-Leichsenring KR, Junginger A, Olaka LA, Tiedemann R,
Trauth MH (2011) Environmental variability in Lake Na-
ivasha, Kenya, over the last two centuries. J Paleolimnol
45:353–367
Straub F (2002) Apparition envahissante de la diatomee Ach-
nanthes catenata Bily & Marvan (Heterokontophyta, Bacil-
lariophyceae) dans le Lac de Neuchatel (Suisse). Bull Soc
Neuc Sci Nat 125:59–65 (Occurrence of the invasive diatom
Achnanthes catenata Bily & Marvan (Heterokontophyta,
Bacillariophyceae) in Lake Neuchatel, Switzerland)
Valderrama GC (1981) The simultaneous analysis of total
nitrogen and total phosphorus in natural waters. Mar Chem
10:109–122
van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist
and ecological indicator values of freshwater diatoms from
the Netherlands. Neth J of Aq Ecol 28:117–133
Velez MI, Hooghiemstra H, Metcalfe S, Martınez I, Mommer-
steeg H (2003) Pollen and diatom based environmental
history since the last glacial maximum from the Andean
core Fuquene-7, Colombia. J Quat Sci 18(1):17–30
Yang X, Anderson NJ, Dong X, Shen JI (2008) Surface sediment
diatom assemblages and epilimnetic total phosphorus in
large, shallow lakes of the Yangtze floodplain: their rela-
tionships and implications for assessing long-term eutro-
phication. Freshw Biol 53:1273–1290
Zalat AA (2000) Distribution and paleoecological significance
of fossil diatom assemblages from the Holocene sediments
of Lake Manzala. Egypt Diatom Res 15:167–190
766 J Paleolimnol (2012) 48:751–766
123