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Secondary production and biomass of Cladocera in two marginal lakes after the
recovery of their hydrologic connectivity with a tropical river.
Eliana Aparecida Panarelli1, Silvia Maria C. Casanova2 & Raoul Henry2
1
State University of Mato Grosso do Sul, Coxim, MS, Brazil.
State University of São Paulo, Institute of Biosciences, Department of Zoology, P.O
Box 510, 18618-000 Botucatu, SP, Brazil
2
e-mail: epanarelli@ig.com.br; casanova@ibb.unesp.br ; rhenry@ibb.unesp.br
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ABSTRACT: Secondary production and biomass of Cladocera in two marginal
lakes after the recovery of their hydrologic connectivity with a tropical river.
Secondary production and biomass of Cladocera populations were studied in two
marginal lakes whose connection to a tropical river was reestablished after a prolonged
drought period. Cladocera were sampled during two periods: immediately after the river
water inflow to the lakes and 7 months after the re-connection with the river in a period
of hydrologic stability of the lakes. The samples were collected every 48 h for one
month in each period. Secondary production and biomass were compared between lakes
and periods in order to identify the main controlling factors of the variations observed in
Cladocera productivity. Cladocerans were more productive during the first study period,
immediately after the increase in water volume, when high water temperatures were
recorded in the two lacustrine systems. Secondary production and biomass values were
higher in the more eutrophic lake whose the water chemical and physical characteristics
presented slow alterations during the first study period. The lake that had large spatial
heterogeneity and linkage with the river presented high Cladocera richness; however,
secondary production and biomass were low. Variations in the water volume and
temperature and the degree of trophy affected the secondary production and biomass of
the main Cladocera species of the two studied lakes significantly.
Keywords: Secondary production, biomass, Cladocera, marginal lakes.
RESUMO: Produção secundária e biomassa de Cladocera em dois lagos
marginais, após a recuperação de sua conectividade hidrológica com um rio
tropical. A produção secundária e a biomassa de populações de Cladocera foram
estudadas em dois lagos marginais, cuja conexão com um rio tropical foi re-estabelecida
após um período prolongado de seca. A comunidade de Cladocera foi amostrada em
dois períodos: um imediatamente após o influxo lateral de água e o outro, sete meses
após a re-conexão com o rio, num período de estabilidade hidrológica dos lagos. As
amostras foram coletadas cada 48 horas durante um mês em cada periodo. A produção
secundária e a biomassa foram comparadas entre lagos e períodos com finalidade de
identificar os principais fatores controladores das variações observadas na produtividade
de Cladocera. Os Cladocera foram mais produtivos durante o primeiro período de
estudo, imediatamente após o aumento de volume de água, quando altas temperaturas da
água foram registradas nos dois ambientes lacustres. Os valores de produção secundária
e de biomassa foram mais altos na lagoa mais eutrófica, cujas características químicas e
físicas da água apresentaram pequenas alterações durante o primeiro período de estudo.
O lago com maior heterogeneidade espacial e com ampla associação com o rio
apresentou elevada riqueza de Cladocera; entretanto, a produção secundária e a
biomassa foram baixas. Variações no volume da água e temperatura e o grau de trofia
afetaram significativamente a produção secundária e a biomassa das principais espécies
de Cladocera nos dois lagos estudados.
Palavras-chave: Produção secundária, biomassa, Cladocera, lagos marginais.
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Introduction
Cladocerans are recognized as being important for the energy transference from
the food chain base to vertebrate and invertebrate predators in lacustrine environments
(Sarma et al., 2005). Bernardi et al. (1987) pointed out that besides being important
preys for vertebrates and invertebrates, the short generation time and high reproductive
efficiency of cladocerans further enhance the energy transference dynamics through the
food chain. The high reproductive efficiency of Cladocera was also recorded by SaintJean & Bonou (1994) in zooplankton of tropical lakes.
Some Cladocera species are herbivorous, while others, such as Bosmina species,
consume organic matter and bacteria associated to degradation (Loureiro, 1988). Araujo
& Pinto-Coelho (1998) observed that a large extent of the energetic requirement of
zooplankton in Pampulha Reservoir (Minas Gerais, Brazil) is supplied by the detritus
chain, because the phytoplankton primary production is below the carbon assimilation
rates by zooplankton in different periods of the year. Hanazato & Yasuno (1985, 1987)
evidenced that the detritus chain is the main route of energy transference from
phytoplankton to zooplankton during the period with the highest Cladocera production
in Lake Kasumigaura (Japan).
According to Paggi & Jose De Paggi (1990), it is probable that the predation
pressure from small fish on zooplankton is more intense in alluvial valley lentic
environments than in lotic waters, because several species of small planktivorous fish
are found associated with the vegetation of marginal lakes. In addition, these
environments are sites of reproduction of many fish species that endure adult life in
lotic environment, but that feed on marginal lake resident populations during the initial
phases of development.
In a study on the trophic structure of the ichthyofauna of the High Paraná river
floodplain (Brazil), Hahn et al. (1997) observed that micro-crustaceans are food
components of the diet of 17 fish species. According to Agostinho et al. (1997),
Hypophthlamus edentatus is the only exclusive planktivorous in this region. Other fish
feed on plankton mainly in the initial phases of development and as an accessory
resource in the adult stage. Carvalho et al. (2003) showed the predominance of
planktivorous fish in marginal lakes of Paranapanema River. Cladocera was recorded as
an important diet component of several invertebrate taxonomic groups, such as
Chaoborus (Hanazato 1990; Stenson 1990), Mesostoma (Rocha et al., 1990), and some
Cyclopoida species, such as of the Mesocyclops genus, an efficient predator (Dumont et
al., 1990).
Lakes marginal to rivers are highly heterogeneous habitats due to the differences
between bottom topography and the degrees of connectivity with the rivers. These lakes
constitute transition zones between the aquatic and the terrestrial systems, and according
to Junk (1997), they provide an important shelter for aquatic animals. These lakes have
long water residence times when compared to those of river channels and constitute
important development sites of populations adapted to lentic conditions.
Despite the recognized role of zooplankton in the trophic network of aquatic
communities of tropical and subtropical region marginal lakes, studies on secondary
production of Cladocera are rare yet. In a comparison of the production in the great
floodplains of South America, the Amazon River, and the Mato Grosso Pantanal
floodplains, Junk & Silva (1995) reported only fish and other vertebrates with potential
biomass production.
The present study intends to contribute to the understanding of the secondary
production of Cladocera in marginal lakes submitted to hydrologic pulses. The aim is to
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answer two questions: 1) if the secondary production of Cladocera is higher
immediately after the river water inflow into the lakes caused by hydrologic pulse or
after the stabilization of the hydrologic conditions in lacustrine systems, and 2) if the
secondary of Cladocera production is higher in lakes with wide or narrow association
with the river.
Material and methods
1. The study area
The two lateral lakes selected for this study (Lake Coqueiral and Lake
Camargo), have distinct morphometric characteristics and connections with
Paranapanema River (São Paulo, Brazil). They undergo water level variations as a
consequence of the hydrologic regime of the river and of operational management of a
hydroelectric power plant (Jurumirim Reservoir) (Figure 1). Only during a prolonged
drought period (from October 1999 to December 2000) did the two lakes remain
isolated from the river. According to Henry et al. (2005), this unusual drought period
caused environmental stress. The secondary production of Cladocera, biomass, and
density were evaluated in two periods: immediately after the reconnection of the lakes
with river (from January 11 to February 06, 2001) and seven months after the reestablishment of connection (from July 03 to 29, 2001), a period of great hydrologic
stability. The main morphometric characteristics of the two lakes and their degree of
association with the river were described in Henry (2005).
Water was sampled in the limnetic region of the two lakes, near the connection
with the river every 48 h in the two study periods. Dissolved oxygen (Winckler method,
according to Golterman et al. 1978), pH (Micronal B-380 pHmeter), electrical
conductivity (Hach, model 2511 conductivimeter with correction for 25 oC according to
Golterman et al. 1978), suspended organic and inorganic matter (gravimetry, according
to Cole 1979), water and air temperatures (Toho-Dentam ET-3 thermistor), and
transparency (Secchi disk) were measured. The variation of the water volume of the
lakes was evaluated by extrapolation of the hypsographic curve of each environment
presented in Henry (2005) from reservoir stage variations (data supplied by Duke
Energy Company) and from the measurement of the maximum depth of each lake.
Rainfall data were obtained from a pluviometric station in Angatuba Town, located
around 20 km from the study area.
Phytoplankton biomass was estimated from the total pigment
(chlorophyll-a and phaephytin) concentration (Golterman et al., 1978). An integrated
sample of the zooplankton community was obtained by filtration of 100 to 500 L of
water with a suction pump (from the surface to 0.5 m above the sediment) and a 50-μm
mesh net. Then, the organisms were anaesthetized with CO2 saturated water solution
and fixed with 4% formaldehyde.
In laboratory, the density of cladocerans was counted (ind.m-3). To
determine biomass, 30 organisms of each species in different stages of development,
adult, juvenile, and neonate, were measured under microscope at 100X magnification.
Cladocera dry weight biomass was calculated using length-mass equations (McCauley,
1984; Dumont et al., 1975; Bottrell et al., 1976). The egg weight was obtained from
Dumont et al. (1975) and Melão (1997). The P:B ratio and renewal time (1/P:B) were
computed according to Winberg (1971). The secondary productivity was calculated by
the production estimation method of populations with continuous reproduction
(Winberg et al., 1971; Winberg 1971). The time of egg development was estimated
according to Bottrell et al. (1976) and the duration time of all other development stages
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was obtained in literature (Bohrer, 1995; Melão, 1997; 1999; Rietzler, 1998; SantosWisniewski, 1998). These authors obtained the development times of some Cladocera
species at two different temperatures. The resulting temperature coefficient (Q10),
according to the Van’t Hoff – Arrhenius law, allowed estimating the development time
for the temperatures recorded in the two lakes. Q10 was obtained through the following
equation: Q10 = (K1/K2) 10/(T2 – T1), where K1 and K2 are the velocities of the biological
process (in this case, development) at two determined temperature in o C.
Student test (t) was used to compare the density, biomass, and productivity of
the Cladocera species of the two lakes. The same variables for the two periods and of
each lake were compared using the t test for dependent variables. Pearson correlations
were computed at significance (P < 0.05) to determine the relationship between the
productivity of the main species and the environmental variables (transformed data:
log10 n +1), (Crow et al., 1960).
Results
Figure 2 shows the variations of the stages of the Paranapanema River and
monthly rainfall. The recovery of the hydrologic connectivity of the two marginal lakes
with the river is indicated (overflow above 563.60 m).
The water mean temperature during the first period varied between 26 and 30 oC
and in the second, it ranged from 15 to 19 oC (Table I). The dissolved oxygen content
and the water pH were higher in Lake Camargo than in Lake Coqueiral in both studied
periods. In Lake Camargo, electrical conductivity was larger than in Lake Coqueiral
during the first period, in contrast to the second period. Organic and inorganic
suspended matter concentrations, water transparency and total pigments were higher in
Lake Coqueiral in the first period, while in the second period, the values were higher in
Lake Camargo.
In January, the lake depth and volume increased gradually (Figure 3). The
increase in volume of Lake Coqueiral was around 500,000 m3 and that of Lake Camargo
was 200,000 m3. During the second period, small variations were observed in lake
volume and depth (Table I; Figure 3).
Fifty-two Cladocera species were found in the two studied environments in both
periods (Table II). In Lake Camargo, 18 Cladocera species were recorded during the
first period and 26 in the second. Higher Cladocera richness was found in Lake
Coqueiral (40 and 37 species in the first and second periods, respectively); 16 species
were common to the two lakes in the first period and, 21 in the second one (Table II).
The total density of Cladocera was significantly higher in Lake Camargo than in
Lake Coqueiral, especially in the first period (t = 6.41; P = 0.000), when it was also
observed a large density range (from 56,010 to 342,186 ind.m-3) in Lake Camargo
(Figure 4). The density of Lake Coqueiral varied from 82 to 4,236 ind.m-3 in January.
During the second period (July), it was observed a progressive increase in Cladocera
density in Lake Camargo, around 40-fold from the beginning to the end of the period
(from 3,278 to 233,351 ind.m-3). The density of Lake Coqueiral fluctuated extensively
(from 40 to 643 ind.m-3) and was higher in the second half of this period. The mean
density of the two environments was higher in January, but significant differences
between periods were observed only in Lake Coqueiral (Table IV).
In Lake Camargo, Bosmina longirostris (mean relative abundance of 44%),
Diaphanosoma birgei (31%) and Ceriodaphnia cornuta v. rigaudi (20%) were the most
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abundant species. During the second period, Bosminopsis deitersi (65%), D.birgei
(15%), and B. longirostris (11%) were dominant in Lake Camargo,
During the first period, Ilyocryptus spinifer (mean relative abundance: 32%),
Chydorus pubescens (20%), Diaphanosoma brevireme (14%), and C. cornuta v. rigaudi
(13%) presented the highest relative abundance in Lake Coqueiral. In July, B. deitersi,
D. brevireme and Alona rectangula (both with 12% relative abundance) were the most
abundant cladocerans (25% mean relative abundance along the period), and the others
had relative abundances <10%.
Cladocera biomass was 168-fold as high in Lake Camargo as in Lake Coqueiral
in the first period and 309-fold as high in the second period. The intra-lake biomass of
Cladocera was higher in the first period in both lakes (Table IV).
The highest biomass of Lake Camargo was recorded for D. birgei, B.
longirostris, and C. C. rigaudi in January and for B. deitersi (Table III) in July.
In Lake Coqueiral, Diaphanosoma brevireme, Ilyocryptus spinifer, Chydorus
pubescens, C. c. rigaudi, Moina micrura, and Diaphanosoma spinulosum presented the
highest biomass in the first period (Table III), while in July, B. deitersi, Bosmina
tubicen, D. brevireme, and Alona rectangula presented the highest biomass values.
Daily secondary production was significantly higher in Lake Camargo than in
Lake Coqueiral in both periods (t = 8.37 and P = 0.000; t = 3.60 and P = 0.003, first and
second periods, respectively). The secondary production of Cladocera of both lakes was
significantly higher in the first period than in the second one (Table IV).
The majority of the total secondary production of Lake Camargo was limited to
some species. In Lake Coqueiral, a higher species number contributed to a larger
Cladocera production (Table V).
The highest secondary production values were recorded for Diaphanosoma
birgei (66% of total production) in Lake Camargo during the first period. Besides the
large egg production, its productivity was higher in the juvenile stage than in the adult
stage due to the body mass gain (Table V). Although little productive in Lake Coqueiral
in January, two congeneric species, D. brevireme and D. spinulosum had a large
participation in the production of this lake in July, with mean productions of 17 and 7%,
respectively.
In the second period (July), Bosmina longirostris was the second most
productive species (18% of total) of Lake Camargo, but with a large part of the energy
directed to egg production. Ceriodaphnia cornuta v. rigaudi also presented large egg
production (6% of total) in January. M. micrura also showed relatively high production
(8% of total), but the energy was directed mainly to body mass gain between the
juvenile and the adult phases (Table V).
The littoral Cladocera species found exclusively in Lake Coqueiral in the first
period (January) were highly productive (Chydorus pubescens and Ilyocryptus spinifer
with 31% and 23% of total production, respectively).
In the second period (July), Bosminopsis deitersi was the most productive
species of Lake Camargo (63%) and Lake Coqueiral (33%). In both environments, egg
production predominated in relation to body mass production (Table V). Diaphanosoma
birgei was the second most productive species in Lake Camargo (17% of the total
production), followed by Bosmina longirostris (13%). In Lake Coqueiral, other
components of the Bosmina and Diaphanosoma genera presented significant
productivity values (B. tubicen with 13%, B. hagmanni with 6%, D. spinulosum with
7%, and D. brevireme with 6% of the total production).
During the first study period, the P:B ratio of Lake Coqueiral was higher (mean:
1.288), with a low population renewal time (mean of 0.8 days), while the mean P:B of
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Lake Camargo was 0.478 with a population renewal time of 2.1 days. The mean P:B
ratios of Lake Coqueiral and Lake Camargos in the second period were 0.171 and
0.151, respectively, and the renewal time was around 6 days.
Correlations between the productivity of Diaphanosoma birgei and water
temperature (r = -0.578); the productivity of Bosmina longirostris and lake volume
(r = -0.593), dissolved oxygen (r = +0.589), electrical conductivity (r = + 0.531) and
inorganic suspended matter (r = +0.579); and the productivity of Ceriodaphnia cornuta
v. rigaudi and water temperature (r= -0.687), pH (r= -0.528) of Lake Camargo were
significant in the first study period (January). In the same period in Lake Coqueiral, the
productivity of Diaphanosoma brevireme presented significant correlations with lake
volume (r = +0.862), dissolved oxygen (r = -0.816), pH (r = -0.711), electrical
conductivity (r = -0.627) and total pigments (r = -0.610). The correlations between the
productivity of Ilyocryptus spinifer and lake volume (r = +0.641), dissolved oxygen (r
=-0.578), pH (r = -0.563), electrical conductivity (r = -0.687) and total pigments (r= 0.548) were also significant.
No significant correlation was found between environmental variables and the
most productive species of Lake Camargo in the second period. In Lake Coqueiral, the
productivity of Bosminopsis deitersi in July correlated significantly with water
transparency (r = 0.517); and those of Bosmina hagmanni and B. tubicen, with organic
suspended matter (r = -0.690 and r = -0.548, respectively), while the productivity of B.
tubicen correlated with dissolved oxygen (r = -0.645) and that of Diaphanosoma
spinulosum with electrical conductivity (r= +0.563).
Discussion
This study was started after the recovery of the hydrologic connectivity between
the Paranapanema River with two marginal lakes after a prolonged drought of 14
months that kept the lacustrine systems isolated from the watercourse (Henry, 2005;
Henry et al., 2005). In early January, 2001 the increase in water level caused a
progressive increase in the volume of the lakes. Lake Coqueiral, which remained
segmented in some isolated water bodies during the drought, became a single system
(De Nadai & Henry, in press). However, Lake Camargo did not present fragmentation
during drought, but its volume and area increased with the water inflow from the river
as well. The volume of each lake had doubled in late January and both were
hydrologically stable in July.
The water characteristics of Lake Camargo changed gradually after the
reconnection with the river, but in the initial phase of water inflow, Cyanophyceae
blooms were observed. Maia-Barbosa & Bozelli (2006) also verified an increase in
phytoplankton density and more eutrophic characteristics in the low water period in
Lake Batata (Amazonas, Brazil).
After the water lateral inflow from the Paranapanema River, low transparency
and high concentration of suspended matter concentration were recorded in both lakes.
In Lake Camargo, the alterations were reduced by dilution effect due to the volume
increase along the first period (January), while in Lake Coqueiral, the water
characteristics were maintained, because of the intense decomposition of the large
amount of submerged plants present in exposed sediment during the prolonged drought
period.
In July, small alterations in volume and environmental variables were observed
in both lakes. The differences observed in water conditions between the two lakes were
small, except for dissolved oxygen concentration, which remained relatively low in
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Lake Coqueiral. According to Thomaz et al. (1997), the variability of limnological
factors is reduced when there is a large influence of a river on lateral lacustrine
environments, since the inundation pulse functions as a homogenizing factor of
floodplains. The same was observed for community characteristics such as those of
Cladocera species in Lake Camargo and Lake Coqueiral, since the largest number of
species common to the two systems was found during the period with the largest water
volume.
The highest Cladocera richness was observed in Lake Coqueiral after the
connection of the aquatic “segments”. The connection of the lake segments was due to
the lateral water inflow from the Paranapanema River (De Nadai & Henry, in press).
Besides the considerable spatial heterogeneity in the period before the water inflow
from the river, large temporal modifications of the lake characteristics were recorded.
The spatial and temporal heterogeneity provided the Cladocera community with diverse
opportunities to develop a large number of species. In typical floodplains, high spatial
and temporal heterogeneity is a determining factor of high species richness (Ward et al.,
1999).
The large expansion of macrophyte stands (with a predominance of Eichhornia
azurea) during the period before this study favored the colonization by littoral
Cladocera species. After the re-establishment of the connectivity of the Paranapanema
River with Lake Coqueiral, the introduction of species by drift caused an increase in the
richness of planktonic species (De Nadai & Henry, in press).
The comparison of the composition of Cladocera families, the highest richness
was found for Chydoridae (28 species). Rocha et al. (2002) pointed out that this family
is the most important one in terms of species richness in the littoral zones of limnetic
systems of São Paulo State (Brazil). It was recorded in marginal lakes of Mogi-Guaçu
River (Santos-Wisniewski et al., 2000), as well in marginal lakes of Cuiabá River, Mato
Grosso state (Neves et al., 2003), and in the floodplains of the Alto Paraná River
(Lansac-Toha et al., 1997).
The large species richness of Lake Coqueiral revealed a large relative
participation of Cladocera in the total biomass and productivity during the two study
periods. In contrast, most of the Cladocera abundance in Lake Camargo was limited to a
few species from three families (Bosminidae, Sididae and Daphniidae) composed by
typically limnetic genera.
The total secondary production of Cladocera in Lake Camargo and Lake
Coqueiral were the highest and the lowest, respectively, comparatively to those of other
lacustrine environments of Brazil (Table VI). It had an increasing trend from
oligotrophic (Lake Dourada, São Paulo) to eutrophic (Barra Bonita Reservoir, São
Paulo).
Sendacz et al. (2006) compared the zooplankton biomass values of two
reservoirs in Alto Tietê Basin (São Paulo, Brazil) with those of two distinct trophic
status environments and found that the Cladocera biomass in the oligotrophic reservoir
was high even when numerically dominated by rotifers. Cladocera biomass ranged from
37,727 to 69,598 μgDW.m-3 in Guarapiranga Reservoir, a eutrophic system, and from
9,265 to 9,794 μgDW.m-3, in Ponte Nova Reservoir, an oligotrophic system, both
in the São Paulo metropolitan region (Sendacz et al., 2006).
In the highly eutrophic system of Lake Kasumigaura, Japan, the productivity of
Cladocera varied between 4.2 and 13.1 gDW.m-3 .year-1 (Hanazato &Yasuno, 1985).
This value corresponds to 23,700 μgDW.m-3.day-1, similar to that recorded by SantosWisniewski & Rocha (2007) for copepods (23,600 μgDW.m-3.day-1) in Barra Bonita
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Reservoir, a eutrophic reservoir in São Paulo State, Brazil. The mean productivities of
Lake Camargo in the two periods (18,300 μgDW.m-3.day-1) were similar.
In January, Diaphanosoma birgei presented a very high secondary production in
Lake Camargo and a large part of the energy was directed to body mass gain. Bosmina
longirostris was the second most productive species, but a large proportion of the
energy was used in egg production and body mass gain. Maia-Barbosa & Bozelli (2006)
found that the predominance of D. birgei and Bosmina hagmanni in Lake Batata
(Amazonas) in the low water period was due to its ability to feed on filamentous algae
and cyanophyceae in eutrophic conditions.
In this study, a high availability of energy to feed Cladocera was recorded in
January due to the large concentration of suspended organic matter resulting from the
degradation of terrestrial vegetation after the lateral water inflow from Paranapanema
River, especially into Lake Coqueiral. Besides its direct use of decomposing matter as
food, Cladocera can release secondary metabolites that either stimulate or inhibit its
population development. In an experimental study on the influence of diet on the
growth and development of Cladocera populations, Sipauba-Tavares & Bachion (2002)
obtained high longevity and spawning for D. birgei in algae culture enriched with B
complex vitamin. This may indicate that besides food quality, the presence of secondary
metabolites may stimulate Cladocera production. In natural environments, B vitamin
arises from bacteria metabolic processes, some phytoplankton species, and the autolysis
of senescent cells. Santos et al. (2006) verified experimentally that the addition of
humic substances to a Ceriodaphnia silvestrii culture resulted in better development,
growth, reproduction, and survival of the species.
Bosminopsis deitersi, the most productive species in the two lakes in July,
predominated in Lake Camargo, but in Lake Coqueiral, the Cladocera community
presented relative abundance <50%. In another lake (Lake Dourada), B. deitersi
presented the highest productivity during the rainy season (Melão & Rocha, 2006). The
absence of B. deitersi in Lake Camargo and its low density in Lake Coqueiral in
January is an intriguing fact. Santos-Wisniewski et al. (2000) related B. deitersi to
oligotrophic and limnetic environments. In a characterization of longitudinal gradient of
zooplankton assembly upstream and downstream Jurumirim Reservoir (São Paulo,
Brazil), Panarelli et al. (2003) concluded that B. deitersi is a typically fluvial species. In
contrast, Lansac-Toha et al. (1997) and Rossa et al. (2001) pointed out that B. deitersi is
one of the most abundant Cladocera species in the floodplains of Paraná, being frequent
in lentic, semi-lotic, and lotic environments. Probably, the B. deitersi record limited to
the second period of this study was related to more stable environmental conditions.
The Diaphanosoma genus composed of D. brevireme and D. spinulosum in Lake
Coqueiral, presented a significant productivity in the second period of study. In Lake
Camargo, D. birgei was the third most productive species, but it presented lower
production than that of January. The variation of the production of D. birgei in Lake
Camargo is similar to that of a congeneric species (D. excisium) dominant in a eutrophic
lake of Ethiopia, whose production ranged from 20,800 to 213 μgDW.m-3.day-1
(Mengestou & Fernando, 1991).
Ilyocryptus spinifer and Chydorus pubescens were the littoral cladocerans that
presented the highest productivity in Lake Coqueiral in January. According to SantosWisnieewski et al. (2002), Chydoridae contribute significantly to the productivity of
bodies of water. In the case of Lake Coqueiral, the water lateral inflow from the river
may revolve the sediment and resuspend I. spinifer in the water column and drain of
macrophytes in the littoral to the pelagic zones.
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The coexistence of Moina species is common in tropical regions (Dumont,
1994), such as occurred in Lake Camargo in January, when M. minuta and M.micrura
were recorded. M. reticulata was found only in Lake Coqueiral and in the absence of
the other two species. Moina presented low densities in the second study period (July)
in oligotrophic conditions. Santos-Wisniewski et al. (2002) pointed out that M. minuta
had wide distribution in oligo-mesotrophic environment, being substituted by M.
micrura with an increase in eutrophication. According to Keppeler & Hardy (2002), the
production of M. minuta may vary with natality and mortality rates in the high water
period in Lake Amapá (Acre, Brazil). The authors also observed that this cladoceran
used a large part of the energy in body mass gain and a small part in egg production. A
similar observation was evidenced in Lake Camargo in January for M. micrura, which
used >95% of its production in body mass gain.
In Cladocera populations, responses to environmental variations may be fast due
to its short time of development and reproduction by parthenogenesis, when the
environmental conditions are favorable. After the occurrence of an environmental stress
period, such as observed before this study (a prolonged 14-month drought), the increase
in productivity may reflect resting egg hatching. The flooding of the shallow lake areas
probably produced the emergence of organisms that remained in resting form during the
drought period. Panarelli et al. (2008) showed the importance of resting eggs to recover
the zooplankton community in a lake isolated from the river in the same region by a
severe drought. In an experimental study, we observed egg hatching for three Cladocera
species (Alona intermedia, Ceriodaphnia cornuta, and Diaphanosoma birgei) present in
sediment. After the lake filling, 12 Cladocera species were recorded, probably also
arising from resting eggs, since the lake was not connected to the river.
The productivity of the majority of Cladocera species in July was favored by
water inflow from the river to the lakes because of the recorded direct relationship
between productivity and the increase in lake volume recorded, except for Bosmina
longirostris and Diaphanosoma birgei. Hanazato & Yasuno (1987) pointed out that
production was higher in shallow zones of Lake Kasumigaura (Japan), suggesting that
detritus resuspension from the bottom caused an increase in zooplankton production,
dominated mainly by B. fatalis, D. brachyurum, and B. longirostris in this order.
The productivity of Cladocera species in Lake Coqueiral is affected either
positively or negatively by hydrologic factors (such as lake volume) and water chemical
factors (such as dissolved oxygen, pH, and electrical conductivity) factors as the
correlation study showed. Water inflow to the lakes in the first period favored the
productivity of the majority of the populations, but the environmental modifications in
water produced a decrease in the productivity of some species. Feeding and temperature
are two environmental factors that greatly influence zooplankton production in
temperate zones (Shuter & Ing, 1997; Stockwell & Johansson, 1997). According to
Sarma et al. (2005), Cladocera population growth rate is affected by the interaction
between temperature and food availability, and tropical species are more influenced by
variations in food concentration than temperate species are. Melão (1999) pointed out
that the number of eggs produced had a direct relation with food supply and quality.
Amarasinghe et al. (1997) reported that many temperate, tropical, and
subtropical lakes and reservoirs showed a significant positive correlation between
micro-crustaceans and phytoplankton biomass. A negative correlation was recorded
between phytoplankton biomass and the productivity of some Cladocera species in Lake
Coqueiral in January. Hart (1987) verified that the concentration of chlorophyll-a
influenced the natality rate of herbivorous zooplanktonic crustaceans in Lake Le Roux
(South Africa) and the mortality rate of three Cladocera species positively. According to
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Hart (1987), this apparent contradiction must to be attributed to phytoplankton density
and to algae composition.
The highest secondary production in Lake Camargo and the highest renewal rate
of Cladocera populations occurred in more eutrophic conditions when Cyanophyceae
blooms were observed. In apparently less eutrophic conditions, when the lake water
level was maximum and the density of Cyanophyceae was apparently low, only one
species (Bosminopsis deitersi) presented high secondary production.
The mean population renewal time (around 6 days) of the two lakes in July was
similar to that recorded by Melão (1997) in Lake Dourada in cold temperature periods.
During the first period (January), the mean population renewal time values were one
day shorter. The fast population renewal is related to the high temperature in this period
of the year and the increase in density due to resting egg hatching, especially in Lake
Coqueiral, where the association with the river caused an increase in surface area.
Gras & Saint-Jean (1983) compared zooplankton production data of Lake Chad
(Africa) and found P:B values varying from 0.02 to 0.45 for temperate lakes and from
0.20 to 0.87 for tropical and subtropical lakes. The renewal rate found for Lake
Camargo is similar to that of temperate lakes. However, for Lake Coqueiral, the mean
value in January surpasses the variation of tropical and subtropical lakes.
In general, it was shown that the population dynamics and the secondary
production of Cladocera in the lakes and periods studied were considerably distinct. In
Lake Camargo, a lake submitted to low river influence and water physical and chemical
variations, the secondary production was higher and limited to the participation of a low
number of typically limnetic species. In Lake Coqueiral, a lake with a large water
exchange with the river, thus highly dynamic, higher species richness, lower dominance
and lower secondary production were observed.
The re-establishment of the hydrologic connectivity between the river and the
lakes in January promoted high secondary production of Cladocera in the two
environments, probably because of the recovery of activity of many latent organisms
and because organisms that invested energy to remain below stress during to the
drought direct the available energy to reproduction in more favorable environmental
conditions. In the second period, seven months after the re-establishment of the
connection between the lotic and lentic systems, differences in the dynamics of
Cladocera populations between the two lakes remained, even with a lower number of
common species and lower differences between the water characteristics of the two
lakes. In this period, the lowest productivity of Cladocera may be due to the more
oligotrophic conditions, but also to the lowest temperature values observed since the
highest renewal time of populations occurred in July.
Acknowledgments
We are grateful to FAPESP (Proc. 97/04999-8 and 99/08748-5) and CNPq (proc.
141.360/2000-3), Dr. Julio César Voltolini (Taubaté University), Hamilton A.
Rodrigues, and Laerte José da Silva, for the financial support, statistical analysis, field
assistance and the revision of the English language, respectively.
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ambientes aquáticos e influência dos níveis fluviométricos. In: Vazzoler, A. E. A. de M.,
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Agostinho, A.A. & Hahn, N. S. (eds). A planície de inundação do Alto Rio Paraná:
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aspectos físicos, biológicos e socioeconômicos. EDUEM, Maringá, pp.
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Ward, J. V. & Stanford, J. A. 1995. Ecological connectivity in alluvial river ecosystems and its
disruption by flow regulation. Regul. Rivers: Res. Mgmt., 11:105-119.
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ecotones and connectivity. Regul. Rivers: Res. Mgmt., 15:125-139.
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Winberg, G. G., Patalas, K., Wright, J. C., Hillbricht-Ilkowska, A., Coope, W. E. & Mann, K.
31
H. 1971. Methods for calculating productivity. In: Edmondson, W. T. & Winberg, G. G.
32
(eds). A manual on methods for the assessment of secondary productivity in fresh waters.
33
IBP Handbook no 17, Blackwell Scientific Publications, Oxford, pp.1-357.
16
Table I: Mean and standard deviation of environmental variables of Lake Camargo and
Lake Coqueiral in the two studied periods (January and July 2001).
Lake Coqueiral
Variable
o
Water temperature ( C)
Lake volume (m3)
Depth (m)
Transparency (m)
-1
Dissolved oxygen (mg L )
pH
-1
Electrical condutivity (µS cm )
-1
Suspended matter (mg L )
Lake Camargo
First period
Second period
First period
Second period
26.71 ± 0.66
16.30 ± 0.98
28.81 ± 1.19
17.41 ± 0.94
555,776 ± 155,489
1,104,123 ± 0
349,127 ± 575,515
547,099 ± 0
1.85 ± 0.47
2.68 ± 0.12
1.99 ± 0.61
3.01 ± 0.08
0.52 ± 0.18
1.58 ± 0.34
0.81 ± 0.32
1.29 ± 0.24
4.25 ± 1.27
5.77 ± 1.08
4.96 ± 1.02
7.34 ± 0.71
6.88 ± 0.19
6.59 ± 0.15
7.12 ± 0.14
6.71 ± 0.14
62.54 ± 7.09
77.11 ± 4.65
95.15 ± 6.09
72.34 ± 3.36
13.14 ± 8.57
2.49 ± 1.31
8.88 ± 10.53
3.40 ± 1.25
Organic fraction(mg L-1)
4.18 ± 2.29
1.25 ± 0.36
2.58 ± 2.19
1.44 ± 0.28
Inorganic fraction (mg L-1)
8.96 ± 7.45
1.24 ± 1.04
6.29 ± 8.42
1.96 ± 1.08
13.77 ± 14.17
5.75 ± 1.72
9.89 ± 3.57
6.69 ± 11.02
-1
Total pigments (µg L )
17
Table II: Cladocera species recorded in each period (January and July 2001) in the two
studied lakes.
.
First period
Lake Camargo
Ceriodaphnia cornuta v. cornuta Sars, 1886
Daphnia gessneri Herbst, 1967
Present in the two environments
Bosmina hagmanni Stingelin, 1904
Bosmina longirostris (O.F. Müller, 1875)
Ceriodaphnia cornuta v. rigaudi Sars,1886
Ceriodaphnia cornuta v. intermedia Sars,1886
Ceriodaphnia silvestrii Daday, 1902
Chydorus pubescens Sars, 1901
Diaphanosoma birgei Korineck, 1981
Diaphanosoma brevireme Sars, 1901
Diaphanosoma fluviatile Hansen, 1899
Diaphanosoma spinulosum Herbst, 1962
Euryalona orientalis (Daday,1898)
Kurzia polyspina Hudec, 2000
Moina micrura Kurz, 1874
Moina minuta Hansen, 1899
Macrothrix squamosa Sars, 1901
Macrothrix superaculeata (Smirnov, 1992)
Second period
Lake Camargo
Alona verrucosa Sars, 1901
Ceriodaphnia cornuta v. intermedia Sars,1886
Chydorus eurynotus Sars, 1901
Oxyurella ciliata Bergamin, 1939
Simocephalus cf. vetulus (O. F. Müller, 1776)
Lake Coqueiral
Acroperus harpae Baird, 1843
Alona cf. affinis (Leydig, 1986)
Alona cf. davidi Richard, 1895
Alona intermedia Sars, 1862
Alona glabra King, 1853
Bosmina longirostris (O.F. Müller, 1875)
Camptocercus dadayi Stingelin, 1913
Dunhevedia odontoplax Sars,1901
Graptoleberis occidentalis Sars, 1901
Kurzia polyspina Hudec, 2000
Kurzia longirostris (Daday, 1898)
Leydigia ciliata Gauthier. 1939
Moina reticulata (Daday,1905)
Macrothrix superaculeata (Smirnov, 1992)
Nicsmirnovicus incredibilis (Smirnov, 1984)
Notoalona sculpta (Sars, 1901)
Lake Coqueiral
Alona cf. poppei Richard, 1897
Alona cf. davidi Richard, 1895
Alona incredibilis Smirnov,1984
Alona intermedia Sars, 1862
Alona glabra King, 1853
Alona quadrangularis (O.F. Müller, 1875)
Alona rectangula Sars, 1861
Alona sp.
Alonella brasiliensis Bergamin,1935
Bosminopsis deitersi Richard,1895
Chydorus sphaericus (O.F. Müller, 1785)
Chydorus cf. nitidulus (Sars,1901)
Chydorus eurynotus Sars,1901
Disparalona dadayi (Birge, 1910)
Dunhevedia odontoplax Sars,1901
Euryalona brasiliensis Brehm & Thomsen, 1936
Ilyocryptus sordidus (Liévin,1848)
Ilyocryptus spinifer Herrick,1882
Kurzia longirostris (Daday, 1898)
Leydigia ciliata Gauthier, 1939
Moina reticulata Hansen,1899
Notoalona sculpta (Sars,1901)
Simocephalus latirostris Stingelin,1906
Simocephalus serrulatus Koch, 1941
Present in the two environments
Alona rectangula Sars, 1861
Alona broanensis Matsumura-Tundisi & Smirnov, 1984
Bosmina hagmanni Stingelin, 1904
Bosmina tubicen Brehm, 1953
Bosminopsis deitersi Richard,1895
Ceriodaphnia cornuta v. cornuta Sars, 1886
Ceriodaphnia cornuta v. rigaudi Sars, 1886
Ceriodaphnia silvestrii Daday, 1902
Chydorus pubescens Sars, 1901
Chydorus sphaericus (O.F. Müller, 1785)
Daphnia ambigua Scourfield, 1947
Daphnia gessneri Herbst, 1967
Diaphanosoma birgei Korineck, 1981
Diaphanosoma brevireme Sars, 1901
Diaphanosoma fluviatile Hansen, 1899
Diaphanosoma spinulosum Herbst, 1962
Ilyocryptus spinifer Herrick,1882
Macrothrix squamosa Sars, 1901
Moina micrura Kurz, 1874
Moina minuta Hansen, 1899
Simocephalus latirostris Stingelin,1906
18
Table III: Mean biomass (μgDW.m-3) and production (μgDW.m-3.day-1) of Cladocera
populations in lakes marginal to Paranapenama River in the two studied periods
(January and July 2001).
Species
A. broanensis
A. incredibilis
A. intermedia
A. glabra
A. rectangula
B. hagmanni
B. longirostris
B. tubiscen
B. deitersi
C. c. cornuta
C. c. intermedia
C. c. rigaudi
C. silvestrii
C. dadayi
C. eurynotus
C. pubescens
C. sphaericus
D. ambigua
D. gessneri
D.birgei
D. brevireme
D. fluviatile
D. spinulosum
D. odontoplax
E. orientalis
I. spinifer
K. polyspina
M. squamosa
M. superaculeata
M. micrura
M. minuta
M. reticulata
S. latirostris
Rare species
Lake Camargo
First period
Second period
B
P
B
P
7.0
0.5
1837.0
129.5
39615.0
6050.0
3479.0
391.9
35591.0 1899.7
565.0
199.0
26.0
1.1
12.0
0.1
11752.0
2048.0
38.0
1.1
27.0
337.0
22.4
3.0
0.2
15.0
0.4
1269.0
57.3
86.0
3.3
39486.0
22020.0
5256.0
517.2
782.0
251
24.0
1.7
7.0
2.0
30.0
5.4
5.0
0.1
213.0
8.0
2422.0
2533.0
873.0
321.0
19.0
0.7
214.0
32.0
46.0
4.1
Lake Coqueiral
First period
Second period
B
P
B
P
13.0
0.6
2.0
0.8
4.0
0.2
2.0
0.3
2.0
0.0
0.4
0.5
1.0
0.5
23.0
0.7
23.0
1.1
0.4
0.2
38.0
2.3
1.0
0.3
39.0
5.6
61.0
19.5
9.0
0.5
12.0
0.8
7.0
0.1
6.0
0.4
4.0
0.4
73.0
156.6
3.0
0.2
13.0
3.4
1.0
0.0
5.0
1.4
223.0
88.9
11.0
1.0
85.0
33.4
7.0
1.3
2.0
0.5
13.0
5.88
121.0
117.4
1.0
0.3
7.0
3.0
6.0
2.2
1.0
0.0
9.0
1.9
75.0
14.35
14.0
2.96
6.0
0.6
7.0
5.15
6.0
1.5
2.0
3.91
5.0
1.2
19
Table IV: Means and standard deviations of Cladocera density (ind.m-3), biomass
(μgDW.m-3), and production (μgDW.m-3.day-1) in the two marginal lakes and
the two studied periods (January and July 2001).
(n=15)
Lake Camargo
Variables
Density
Biomass
Production
Lake Coqueiral
Density
Biomass
Production
Periods (Means  SD)
st
1 :
133,553.30  20,681.89
2nd:
68,419.40  19,732.18
1st:
95,855.46  13,744.24
2nd:
47,522.38  12,959.82
st
1 :
33,466.24  3,919.02
2nd:
3,136.45  801.98
1st:
986.20  314.62
2nd:
174.89  34.48
st
1 :
569.62  194.63
2nd:
136.15  28.81
1st:
509.80  123.86
2nd:
17.49  3.75
T(a)
2.10
P(b)
0.054
2.15
0.049
8.15
0.000
2.58
0.022
2.19
0.045
3.97
0.001
a) “t” test for dependent variables
b)  = 0.05
20
Table V: Mean secondary production (μgDW.m-3.day-1) for different development
stages of the main Cladocera species (>5% of the total relative abundance) in
each period (January and July 2001) in the Lake Camargo and Lake Coqueiral.
Lake Camargo
Fist period
neonate-juvenile
juvenile-adult
adult (egg)
total
Bosmina longirostris
921.67
3,691.63
1,436.21
6,049.51
Ceriodaphnia cornuta rigaudi
486.16
616.87
945.05
2,048.08
1,491.54
18,779.96
1,748.19
22,019.69
228.48
2,242.45
62.00
2,532.92
Diaphanosoma birgei
Moina micrura
Second period
adult (egg)
total
Bosminopsis deitersi
neonate-juvenile
17.75
420.13
1,461.79
1,899.66
Bosmina longirostris
114.01
155.13
122.74
391.88
Diaphanosoma birgei
95.30
303.08
118.82
517.20
adult (egg)
total
Lake Coqueiral
First period
neonate-juvenile
Chydorus pubescens
Diaphanosoma brevireme
Diaphanosoma spinulosum
Ilyocryptus spinifer
Simocephalus latirostris
juvenile-adult
juvenile-adult
2.28
151.70
2.58
156.56
33.73
36.74
18.42
88.89
0.61
30.66
2.14
33.40
11.29
101.89
4.21
117.39
1.12
44.15
0.00
45.26
Second period
neonate-juvenile
juvenile-adult
adult (egg)
total
Bosminopsis deitersi
0.44
1.41
3.71
5.56
Bosmina hagmanni
0.22
0.15
0.68
1.06
Bosmina tubicen
0.42
0.55
1.30
2.28
Diaphanosoma brevireme
0.27
0.77
0.00
1.04
Diaphanosoma spinulosum
0.00
1.26
0.00
1.26
Simocephalus latirostris
0.05
1.44
0.00
1.49
21
Table VI: Comparison of secondary production and renewal time data of Cladocera
studies conducted in Brazil.
Lake Camargo
Lake Coqueiral
Production
(μgDW.m-3.day-1)
P:B
(minima - maxima)
Period (*)
rainy
dry
33,466
3,036
Period(*)
rainy
dry
0.15– 0.05–0.11
1.05
0.17– 0.05–0.55
2.16
0.01– 0.00–0.46
0.95
0.3–3.3 0.1-1.3
0.16– 0.19–0.48
0.48
510
17
Lake Dourada (limnetic zone)
2,207
606
Barra Bonita Reservoir
Lake Batata (non impacted area)
15,445
180
2,100
660
References
This work
This work
(Melão 1997)
(Santos-Wisniewski 1998)
(Maia-Barbosa 2000)
(Maia-Barbosa, 2000)
Lake Batata (impacted area)
1,780
1,110
(*)
In this study, the first and second periods correspond to rainy and dry periods, respectively.
22
Figure 1: Location of Lake Camargo and Lake Coqueiral in the transition zone of the
Paranapanema River – Jurumirim Reservoir, southeast region of São Paulo
State, Brazil.
23
Figure 2: Variation of the stage (m) of the Jurumirim Reservoir (line) and monthly
rainfall (mm) (bars) from November 2000 to July 2001. The dashed line
corresponds to the frontier between overflow and isolation of the two
Paranapanema River marginal lakes.
Figure 3: Variation of depth (grey area) and water transparency (bars) of Lake Camargo
(above) and Lake Coqueiral (below) in the two studied periods.
24
Figure 4: Variation of Cladocera density (ind.m-3) in Lake Camargo (solid line) and
Lake Coqueiral (dashed line) in the first (above) and the second (below)
periods.
25