问题这个函数错在哪里了？_百度知道http://dx.doi.org/10.-00010
The inverted trophic cascade
in tropical plankton communities: impacts of exotic fish in the Middle Rio Doce
lake district, Minas Gerais, Brazil
A cascata tr&fica invertida em comunidades
planct&nicas tropicais: impactos da introdu&&o de peixes
ex&ticos no distrito de lagos do m&dio rio Doce, MG
Pinto-Coelho, RM.I, ;
Bezerra-Neto, JF.II; Miranda, F.II; Mota, TG.II;
Resck, R.II; Santos, AM.III; Maia-Barbosa, PM.IV;
Mello, NAST.IV; Marques, MM.V; Campos, MO.V;
Barbosa, FAR.V
ILaborat&rio de Gest&o
Ambiental de Reservat&rios, Departamento de Biologia Geral, Instituto
de Ci&ncias Biol&gicas, Universidade Federal de Minas Gerais –
UFMG, CP 486, CEP 3, Belo Horizonte, MG, Brazil
IIPrograma Programa de P&s-Gradua&&o em Ecologia,
Conserva&&o e Manejo da Vida Silvestre, Universidade Federal de
Minas Gerais – UFMG, CP 486, CEP 3, Belo Horizonte, MG, Brazil
IIIDepartamento de Biologia Geral, Centro de Ci&ncias Biol&gicas
e da Sa&de, Universidade Estadual de Montes Claros – UNIMONTES, Rua Rui
Braga, Campus Darcy Ribeiro, CEP 3, Montes Claros, MG, Brazil
IVLaborat&rio de Ecologia do Zoopl&ncton, Departamento
de Biologia Geral, Instituto de Ci&ncias Biol&gicas, Universidade
Federal de Minas Gerais – UFMG, CP 486, CEP 3, Belo Horizonte, MG, Brazil
VLaborat&rio de Limnologia, Departamento de Biologia Geral,
Instituto de Ci&ncias Biol&gicas, Universidade Federal de Minas
Gerais – UFMG, CP 486, CEP 3, Belo Horizonte, MG, Brazil
The present study deals with the ecological impacts
of the introduction of two alien species of piscivorous fish in several lakes
of the Middle Rio Doce lake district in Minas Gerais, Brazil. It was demonstrated
that these effects were not restricted only to the fish community. The introduction
of the predatory red piranha Pygocentrus nattereri and the tucunar&
Cichla cf. ocellaris caused not only a sharp decrease in the number
of native fish species, but also major shifts in other trophic levels. Just
after the fish were introduced, most lakes began to show conspicuous changes
in phytoplankton species composition, in which Cyanophyceae gradually came to
dominate. The zooplankton community lost several species, and in some cases,
such as Lake Carioca, all the cladoceran species disappeared. On the other hand,
invertebrate predators, represented by the dipteran Chaoboridae, boomed in the
lake, with higher densities of exotic species, probably as a result of the "ecological
release" by reduction of the original fish fauna. There was a general trend
of species loss in different trophic levels. All these changes are apparently
associated with decreases in water quality. The present situation in these lakes
demands new approaches to the management and conservation of these ecosystems.
Keywords: exotic species, eutrophication,
trophic cascade, zooplankton, introductions.
O presente estudo trata dos impactos ecol&gicos
da introdu&&o de duas esp&cies invasoras de peixes pisc&voros
em diversos lagos da regi&o lacustre do m&dio rio Doce em Minas
Gerais, Brasil. Demonstrou-se que estes efeitos n&o se restringiram &s
comunidade de peixes. A introdu&&o dos predadores Pygocentrus
nattereri (piranha-vermelha) e Cichla cf. ocelaris (tucunar&)
n&o s& causou uma forte redu&&o no n&mero
de esp&cies de peixes nativos, como tamb&m mudan&as nos
n&veis tr&ficos inferiores. Pouco depois das introdu&&es,
a maioria dos lagos come&ou a mostrar altera&&es na comunidade
fitoplanct&nica, tais como o aparecimento da domin&ncia de Cyanophyceae.
A comunidade zooplanct&nica perdeu diversas esp&cies e, em alguns
casos, houve o desaparecimento de todas as esp&cies de clad&ceros
limn&ticos, como & o caso da lagoa Carioca. Por outro lado, predadores
invertebrados, representados pelos d&pteros da fam&lia Chaoboridae,
floresceram nos lagos com maiores densidades de esp&cies ex&ticas
de peixes, provavelmente como resultado da "libera&&o ecol&gica"
causada pela redu&&o da ictiofauna original. Al&m de uma
tend&ncia geral de perda de esp&cies em diferentes n&veis
tr&ficos, outras mudan&as est&o aparentemente associadas
com a redu&&o da qualidade de &gua. Dessa forma, esses
ecossistemas est&o necessitando urgentemente de novas abordagens nas
estrat&gias de manejo e conserva&&o.
Palavras-chave: esp&cies ex&ticas,
eutrofiza&&o, cascata tr&fica, zoopl&ncton, introdu&&es.
1. Introduction
Increasing ecological damage produced by biological
invasions has begun to occupy a central role in applied ecology and conservation
biology. The ecological effects of biological invasions have been the focus
of a long series of investigations ranging from population-level manipulation
experiments to whole-ecosystem approaches (Simon and Towsend, 2003). Several
well-known examples of catastrophic introductions of alien species are now documented
in the ecological literature. Classical examples of such introductions include
the case of the Nile Perch (Lates niloticus Linnaeus, 1758) in Lake Victoria,
East Africa (Kaufman, 1992), and the introduction of the zebra mussel (Dreissena
polymorpha Pallas, 1771) in the Laurentian Great Lakes (Ricciardi, 2003).
The theory of biological invasions usually predicts that the effects of these
introductions are more intense when the invaders occupy higher trophic levels,
especially when they are top predators. Several well-documented studies have
related the devastating effects of alien top predators in aquatic ecosystems
(Simon and Townsend, 2003; Soto et al., 2006; Bystr&m et al., 2007).
The introduction of alien fish species into tropical
lakes and reservoirs is accepted as one of the major causes of fish species
loss in these ecosystems (Latini and Petrere, 2004). In Brazil, fish introductions
are common in most lakes and reservoirs. In most cases, not only have private
fishing clubs and associations supported these introductions, but several governmental
agencies have also contributed to the spread of several exotic fish species,
especially in the hydroelectric reservoir chains in major rivers in southeastern
Brazil. The idea was to increase fish production in these new artificial lakes
by introducing exotic fishes. Most introductions occurred in the 1960s and 1970s,
and consisted of translocations of fish species from the Amazon basin, such
as the tucunar&, Cichla ocellaris (Agostinho et al., 2005).
In the present study, the effects of introduction
of exotic fish species were investigated in different compartments of the plankton
community in one of the most important lake districts of Brazil, the Middle
Rio Doce. The lakes studied are located within and near the Rio Doce State Park
(Parque Estadual do Rio Doce – PERD). The impacts of these introductions on
the local fish fauna are already well described. The presence of the exotic
piscivorous tucunar& Cichla cf. ocellaris Bloch and Schneider,
1801 and the red piranha Pygocentrus nattereri Kner, 1858 affected the
native fish community, causing the disappearance of some species and a reduction
in the abundance of young individuals of others (Godinho et al., 1994; Latini
and Petrere, 2004). These introductions occurred about 30 years ago, and regular
monitoring of the fish communities in some of these lakes indicates that these
two exotic species are still spreading into new lakes in this area. Most lakes
have connections that can be active, especially during extreme rain events (Latini
et al., 2005).
This investigation aimed to answer the question
as to whether these introductions are affecting other trophic levels in addition
to the native fish species of these lakes. Additionally, we analyzed published
data and gathered new data showing that the introduction of these two piscivorous
fish species contributed to create a zooplankton community structure with the
opposite pattern to that predicted by the trophic-cascade hypothesis (sensu
Carpenter et al., 1985).
2. Material and Methods
2.1. Study areas
The lacustrine region of the Rio Doce Valley
is the largest lake district in Brazil. This unique system is located in a dammed
valley along the middle course of the Rio Doce River, in the state of Minas
Gerais, Brazil (CNPq/PELD, 2007). In this area, there are approximately 130
lakes, 42 of them located within the Rio Doce State Park (PERD), which has an
area of 36,000 ha and preserves the largest remaining fragment of the Atlantic
Forest in the state of Minas Gerais (Latini et al., 2005). The other lakes are
located outside the park, where their original catchment basin has been drastically
altered by human activities over the last 30 years. Most of the lakes are now
surrounded by monocultures of Eucalyptus spp.
In the present study, seven lakes were considered:
Dom Helv&cio, Carioca, Gambazinho, Jacar&, Amarela, Palmerinha,
and &Aguas Claras. The first three lakes are located inside the PERD.
These lakes have different morphometric as well as limnological features (). These are generally small, shallow lakes (Surface & 5 km2
and Zmax & 10 m). The exception is Lake Dom Helv&cio, with
a total area of 5.27 km2 and Zmax of 39.3 m (Pinto-Coelho
et al., in preparation).
2.2. General methods
Between August 2004 and September 2005, seven
lakes (three lakes in the PERD and four lakes outside it) were studied during
the dry (July 2004) and rainy seasons (January 2005). A multi-probe (HORIBA,
model U-22) was used to measure water temperature, pH, dissolved oxygen concentration,
and electrical conductivity at a central point in each lake, covering the entire
water column. Further samples were taken with a 2.0 L Van Dorn sampler for nitrate,
ammonium, total phosphorus, and chlorophyll-a determinations as well
as for phytoplankton counts. On the day of sampling, two replicate samples of
water were filtered through 47 mm GF-C Whatman filters. The filtrate was transferred
to a clean 500 mL bottle for inorganic-nitrogen analyses, and the glass-fiber
filter was reserved for chlorophyll-a determinations (Lorenzen, 1967).
All samples for chemical analyses were stored at –25 °C (conventional freezer)
until further processing (APHA, 2000).
The phytoplankton samples were collected and
preserved in acetic lugol. The density of algal individuals was determined using
the inverted-microscope method (Uterm&hl, 1958). Integrated triplicate
additional samples for taxonomic identification of phytoplankton were also taken
with a conical net (20 µm
mesh size), preserved in 8% buffered formalin, and identified according to the
classic literature. Zooplankton was sampled in replicates using two conical
nets of different mesh sizes: 68 µm
(microzooplankton) and 200 µm
(mesozooplankton). Organisms were fixed in 4% sucrose-formalin solution buffered
to pH 7.0, containing the vital stain Rose Bengal.
Fish were sampled in seven different lakes. We
used gill nets (10 m long by 1.5 m wide) with the following mesh sizes: 3, 4,
5, 6, 8, 10, and 12 cm. The nets were deployed perpendicularly to the lakeshores
at 06:00 PM until the next day, when they were retrieved at 08:00 AM (14 hours
of exposure time). The collected specimens were sorted by mesh size and immediately
fixed using 10% formalin. The fixation solution was changed to 70% ethanol one
week later. In the laboratory, all individuals were identified, measured (mm),
and weighed (fresh weight, in grams). The results were expressed using the CPUE
biomass and numbers of individuals standardized for 100 m2 gill-net
We also compared our data to other sources in
the literature and to other data from digital libraries such as the data bank
of the long-term ecological program conducted in the region (CNPq/PELD, 2007)
and the data bank on freshwater resources of the Rio Doce (FAPEMIG/Rio Doce,
2.3. Data analysis
The quantitative differences in fish community
structure between lakes were investigated by co-occurrence analysis. A module
of the EcoSim program (Gotelli and Entsminger, 2001) was used. The co-occurrence
module tests for non-random patterns of species co-occurrence in a presence-absence
matrix. We used the C-Score test, which measures the tendency for one species
to avoid another. A checkerboard unit is any submatrix of the form:
The number of checkerboard units (CU) for each
species pair is estimated as:
where is S is the number of shared sites (sites
containing both species), and ri and rj are the row totals
for species i and j. The C-score is the average of all possible checkerboard
pairs, calculated for species that occur at least once in the matrix. The larger
the C-score, the less the average co-occurrence among species pairs. In a competitively
structured community, the C-score should be significantly larger than expected
by chance (Gotelli and Entsminger, 2001).
A detrended correspondence analysis (DCA) was
used to investigate possible associations between fish fauna and zooplankton.
A data matrix of fish (CPUE-biomass) and zooplankton abundance was analyzed
together, to identify clusters of lakes of similar structure of zooplankton
and fish communities, and to explore any underlying spatial gradient in species
composition. Data were log-transformed (ln x+1) because of the skewed distribution
of the original data set.
3. Results
In our samplings, all the lakes had very low
nitrate concentrations (& 10 µg.L–1,
), but ammonium exceeded 100 µg.L–1
in most lakes, during the dry season. Total phosphorus also reached its maximum
seasonal values d concentrations of this nutrient varied
from 20 to 76 µg.L–1
except for the maximum concentration 228 µg.L–1
TP observed in &Aguas Claras Lake. The catchment area of this lake is
completely occupied by a monoculture of Eucalyptus spp. A similar seasonal
pattern, with higher values in the dry season, could also be observed for chlorophyll-a.
The highest concentrations of this algal pigment were found in Carioca (48.6
µg.L–1) and
&Aguas Claras (27.9 µg.L–1),
respectively ().
The Rio Doce lakes differ sharply in the abundance
and species composition of their phytoplankton communities (). The algal species of lakes Carioca, Gambazinho, and Amarela ranged between
43 and 47 Lake Carioca had the fewest species of all the lakes (). Phytoplankton of lakes Dom Helv&cio and Jacar& included
more than 60 different taxa of algae.
Higher algal densities were observed for most
lakes during the rainy season (). In this season,
the total algal densities in lakes Carioca and &Aguas Claras were much
higher than in the other lakes. These two lakes also had the highest chlorophyll-a
concentrations ().
The phytoplankton of some lakes (e.g., Lake Carioca)
had not only a low richness of algal species but also a strong dominance of
Cyanophyceae (). The figure also shows that this
dominance tended to be more pronounced during the rainy season. Other lakes,
such as Gambazinho and Jacar& (dry season) and &Aguas Claras (rainy
season), also had a strong dominance of this group of prokaryotic producers
The zooplankton composition of the Rio Doce lakes
also was structurally simple (, ). The total number of species never exceeded 10 (). In most lakes, this community was dominated by a simple array of small
cyclopoids, cladocerans, and a few rotifers that are commonly found in eutrophic
waters in Brazil. The most commonly observed species were Chaoborus spp.,
Thermocyclops minutus Lowndes, 1934, Bosmina hagmanni Stingelin,
1904, Ceriodaphnia cornuta Sars, 1885, Hexarthra sp., Brachionus
calyciflorus Pallas, 1766, and Filinia sp .
The microzooplankton community (&200 µm)
showed a homogeneous composition in all the lakes. Lakes Carioca, Gambazinho,
and Amarela exhibited the highest densities (rainy season) of the smaller fraction
(). In most cases, this community was dominated
by nauplii of cyclopoid copepods. The mesozooplankton fraction (&200 µm)
also showed higher densities during the rainy season, except for Lake Jacar&
The mesozooplankton in the lakes surrounded by
the Tropical Atlantic Forest within the PERD, such as lakes Carioca and Gambazinho,
was dominated by the copepod cyclopoid Thermocyclops minutus (). Larvae of chaoborids were common in the mesozooplankton of most Rio
Doce lakes, with higher densities observed in lakes &Aguas Claras, Jacar&,
and Carioca during the dry season of 2004 ().
Ostracods were the dominant organisms of this fraction in the lakes situated
outside the Rio Doce Park (lakes &Aguas Claras, Palmeirinha, and Jacar&).
Lake Amarela had a unique mesozooplankton structure, dominated by cladocerans.
It is interesting to note that Chaoborus larvae were few or absent in
this lake ().
It seems that there is an inverse relationship
between density of Chaoborus and the number of taxa of cladocerans in
the lakes (). In these cases, small copepods and
rotifers were the most important organisms of the smaller fraction, and cladocerans
were rare or even absent.
The pattern of high densities of just a few representatives
of zooplankton found for all lakes in this region was not usual only a few years
ago (). We compared our data with some investigations
of zooplankton carried out in Rio Doce lakes in the period 5. This table
suggests that a serious species loss has been occurring in most lakes during
the past 20 years. The zooplankton community of Lake Carioca, for example, is
suffering a steady decrease in species numbers, with the disappearance of all
cladocerans from the limnetic zone (). Moreover,
in Lake Dom Helv&cio, several species such as the calanoids Argyrodiaptomus
furcatus Sars, 1901 and Scolodiaptomus corderoi Wright, 1936, that
were often observed, are now completely absent. Other larger copepods such as
Mesocyclops longisetus Thi&baud, 1912 and Microcyclops
varicans Sars, 1863 and the cladocerans Bosmina coregoni Baird, 1857 and Moina minuta Hansen, 1899 also became extinct in this lake.
As expected from previous studies, we did not
find any exotic fish species in Lake Gambazinho ().
The cumulative biomass of the fish community (CPUE b) in the lakes varied from
3.7 to 8.2 kg (). The highest biomass values (CPUEb
& 3.9 kg) were found for the exotic red piranha in lakes &Aguas
Claras, Carioca, and Dom Helv&cio (). The
exotic Cichla cf. ocellaris is well known for avoiding gill nets
(Godinho and Formagio, 1992), thus the biomass of this species was probably
underestimated. The comparison of relative fish abundance (CPUEn) among all
the lakes also showed the great quantitative importance of exotic fishes in
most lakes (). The native fish species that still
have relative significance were Hoplias malabaricus Bloch, 1794, Oligosarcus
solitarius Menezes, 1987, and Hoplosternum littorale Hancock, 1828.
The Checkerboard score of fish assemblage was
higher than expected by chance (Observed index = 1.76; mean of simulated indices
= 1.57; p observed & expected = 0. permutations). Pygocentrus
nattereri and Hoplosternum littorale exhibited the most antagonistic
behavior (). The impact of exotic fish on native
fish and zooplankton populations is shown by DCA analysis (). Lake Gambazinho, without exotic fish, formed a distinct group with small
native fishes such as Astronotus ocellatus Agassiz and Spix and Agassiz,
1831, Astyanax bimaculatus Linnaeus, 1758, and Oligosarcus solitarius, Ceriodaphnia, calanoid copepodites, and Calanoida. Another group was
formed by Chaoborus larvae, associated with the exotic fishes (Cichla
ocellaris and Pygocentrus nattereri) that prevail in lakes &Aguas
Claras and Carioca ().
4. Discussion
The Phytoplankton of the most Rio Doce studied
lakes is typically a low diverse community with strong dominance of Cyanophyceae.
The zooplankton community is also relatively simple. The total number of observed
copepod and cladoceran species always remained below 10. There was a clear inverse
relationship between Chaoborus abundance and species richness of cladocerans.
We also confirmed a reduced species richness of fish communities in lakes of
the Middle Rio Doce, with a strong dominance of biomass of two alien piscivorous
fish species.
The literature shows, however, that these communities
have never been rich in species. In the early 1980s, four representative lakes
of this region (Dom Helv&cio, Jacar&, Carioca, and Amarela) had
a total fish richness of 25 (Godinho and Vieira, 1998). However, the number
of fish species today is reduced to 3-6 in the same lakes. Most authors agree
that this reduction is a direct result of the introduction of the two piscivorous
fishes Cichla cf. ocellaris and Pygocentrus nattereri (Godinho
et al., 1994, Latini and Petrere, 2004, Latini et al., 2005). Looking at the
high C-score index found in this study, we have clear evidence of the antagonistic
checkerboard pattern between the exotic piscivorous Pygocentrus nattereri
and several native fish species ().
We propose the hypothesis that the changes in
fish community in the lakes of the Middle Rio Doce are inducing further changes
at lower trophic levels. However, this chain of events linked to the introduction
of piscivorous fish in these lakes is contradictory to the predictions of the
trophic-cascade hypothesis (Carpenter et al., 1985): when piscivores are abundant
and planktivorous fish are scarce, zooplankton biomass may be high and dominated
by large species, resulting in higher grazing rates on phytoplankton. This hypothesis,
with some minor modifications, is still the ecological basis for biomanipulation
of most temperate systems (De Melo et al., 1992; Jeppesen et al., 2007).
In the lakes of the Middle Rio Doce, the introductions
of piscivorous fish resulted in an increase in the abundance of invertebrate
predators (Chaoborus). These organisms replaced the planktivorous fish
as major consumers of herbivorous zooplankton. The increase in density of this
invertebrate predator was probably the result of an "ecological release" caused
by the reduction of fish predation. Ecological release is a well-known phenomenon
(Cox and Ricklefs, 1977). It occurs when there is a density increase resulting
from the enlargement of the ecological niche of a species, resulting in decreases
in competition or predation pressure (Losos and Queiroz, 1997).
Innumerable studies have shown that small cladocerans,
rotifers, juvenile copepods (copepodites), and nauplii often dominate the zooplankton
communities in tropical lakes (e.g., Lewis, 2000; Pinto-Coelho et al., 2005).
Chaoborus larvae normally coexist in this environment and are controlled
by fish predation. Originally, the structure of the zooplankton community of
most lakes in the Middle Rio Doce did not differ from this general pattern,
with a general low diversity of microcrustaceans (copepods and cladocerans)
and a numerical dominance of rotifers. However, the introduction of strictly
piscivorous fishes in some lakes is possibly linked to a large species erosion
and diversity decay of microcrustaceans. Today, it is common to find lakes in
the Rio Doce Valley where the zooplankton fauna is reduced to only one species
of copepod (Thermocyclops minutus) with a complete absence of limnetic
cladocerans (e.g. Lake Carioca).
The major effects associated with the introduction
of alien fish species on the ecosystem functioning of the Middle Rio Doce lakes
are summarized in . The introduction of the two
piscivorous fishes caused - at first - a sharp decrease in fish species richness,
with almost all the planktivorous fish becoming locally extinct. The next effect
was the uncontrolled development of Chaoborus populations. This effect
can be seen in lakes Carioca, Palmeirinha, and &Aguas Claras. These lakes
have high proportions of exotic fishes and relatively high densities of chaoborids
in the mesozooplankton (), and in our samples exhibited
the highest seasonal values of chlorophyll-a of phytoplankton. The increase
in density of the invertebrate predators caused a sharp reduction of cladocerans.
Under these circumstances, rotifers, cyclopoid copepodites, and nauplii, associated
with other temporary limnetic organisms such as ostracods, dominated the smaller
zooplankton fraction. Furthermore, these lakes also show a clear biomass accumulation
of primary producers in the lakes, usually represented by cyanobacteria. These
results are contrary to the predictions supported by the trophic cascade hypothesis
(op. cit.), because the increase of piscivory in the Rio Doce lakes actually
led to a reduction of grazing pressure on phytoplankton by zooplankton.
The phenomenon of ecological release affecting
chaoborid larvae can be seen indirectly by considering some behavioral characteristics
of the chaoborids from Rio Doce lakes. The behavior of vertical migration of
zooplankton is widely accepted as a mechanism of evading predators in the water
column (Gliwicz, 1986). Usually, the zooplankton mostly ascends into the epilimnion
at night and migrates down into the colder, darker, and oxygen-poor waters in
the deeper layers at dawn, to avoid predation by visually oriented planktivorous
fish. A strong evidence of the lack of vertebrate predation on zooplankton in
Rio Doce lakes, especially on chaoborid instars, is the total absence of vertical
migration in the populations of Chaoboridae in lakes with exotic fish species,
such as Lake Carioca (Bezerra-Neto, 2007).
Some studies have demonstrated that in lakes
where an extreme enhancement of piscivory occurred ("over-biomanipulation"),
an increase in the abundance of large invertebrate predators can occur, which
then exerts strong predation pressure on herbivorous zooplankton (Wissel et
al., 2000; Bendorf et al., 2000). However, the effects of reduction of fish
predation on Chaoborus larvae become more acute in tropical lakes because:
(1) in these environments, the chaoborids are the only large-bodied zooplankton
invertebrate predators, because other crustacean predators such as Mysis,
Bythotrephes, and Leptodora, common in temperate lakes, are absent
(Fernando, 1994); (2) chaoborids reproduce throughout the year and their life
cycles last approximately 40-60 days, in contrast with 1-2 years in temperate
environments (Bezerra-Neto and Pinto-Coelho, 2002); and (3) bottom-water anoxia
is more common in tropical lakes, which may provide chaoborids with a refuge
from fish predation (Lewis, 2000).
This study demonstrated the effects of the piscivorous
fish invaders on the entire trophic web in some of the most important Middle
Rio Doce lakes. These impacts extended not only to the crustacean zooplankton
but also affected the primary producers. As suggested by the results, future
invasions of Pigocentrus natererii and Cichla cf. ocellaris
will have strong negative effects on fish communities by decreasing the
richness of native fish species and by changing the configuration of entire
ecosystems through top-down cascading effects on the lower trophic levels. Nowadays,
only three lakes within the park reserve do not host alien fish species – Gambazinho,
Azul, and Lagoinha. Outside the reserve, the situation is somewhat better: 13
lakes have their original fish fauna untouched by human activities (Latini et
al., 2005).
The recent ecological changes observed in lakes
of the Middle Rio Doce provide strong evidence of cumulative and synergetic
human factors related to the explosive and unplanned increase in human occupation
in the watershed of one of the most important river basins of southeastern Brazil.
One of the major tasks of ecologists working on impacted areas is attempting
not only to identify but also to understand the major ecological impacts of
different human activities on the existing biota, especially if these impacts
are causing species extinctions. Thus, these findings reinforce the urgency
of improving the strategies of management and conservation of freshwater resources
in the region.
Acknowledgements — We would like to thank
Dr. Liliana Rodrigues and Dr. Janet W. Reid for checking taxonomic determinations
and the improvement of the English writing. We also thank the FAPEMIG (No. 1541/03)
and the Long-Term Ecological Research Program (PELD – CNPq) for supporting this
References
APHA – AMERICAN PUBLIC HEALTH ASSOCIATION. 2000.
Standard Methods for the Examination of Water and Wastewater. 19 ed.
&&&&&&&&[  ]
AGOSTINHO, AA., THOMAZ, SM. and GOMES, LC., 2005.
Conservation of the biodiversity of Brazil's inland waters. Conserv Biol,
vol. 19, no. 3, p. 646-652.
&&&&&&&&[  ]
BENNDORF, J., WISSEL, B., SELL, AF., HORNIG,
U., RITTER, P. and B&OING, W., 2000. Food web manipulation by extreme enhancement
of piscivory: an invertebrate predator compensates for the effects of planktivorous
fish on a plankton community. Limnologica, vol. 30, no. 3, p. 235-245.
&&&&&&&&[  ]
BEZERRA-NETO, JF., 2007. A preda&&o
e a comunidade planct&nica: efeitos diretos e indiretos em corpos aqu&ticos
tropicais. Belo Horizonte: Universidade Federal de Minas Gerais – UFMG.
144 p. [Ph.D. Thesis]
&&&&&&&&[  ].
BEZERRA NETO, JF., PINTO-COELHO, RM., 2002. Population
dynamics and secondary production of Chaoborus brasiliensis (Diptera
- Chaoboridae) in a small tropical reservoir: Lagoa do Nado, Belo Horizonte
(MG). Acta Limnol. Brasil., vol. 14, no.3, p. 145-161.
&&&&&&&&[  ]
BRAND&AO, ECL., BRAZ, SA., BRITO, SL.,
MENENDEZ, RM. and MAIA-BARBOSA, PM., 2002. Flutua&&o mensal do
zoopl&ncton dos lagos Carioca, Dom Helv&cio e Gambazinho (Parque
Estadual do Rio Doce). In BARBOSA, FAR. (Coord.). Relat&rio T&cnico-Cient&fico
das atividades de dezembro de 2001 a agosto 2002 - Pesquisas Ecol&gicas
de Longa Dura&&o (PELD– CNPq) - Sitio 04. Available from: &&&&&&&&[  ]BRITO, SL., VALADARES, CF., MENENDEZ, RM. and
MAIA-BARBOSA, PM., 2002. Estrutura da comunidade zooplanct&nica em tr&s
lagoas do entorno do Parque Estadual do Rio Doce (MG). In: BARBOSA, FAR. (Coord.).
Relat&rio T&cnico-Cient&fico das atividades de dezembro
de 2001 a agosto 2002 - Pesquisas Ecol&gicas de Longa Dura&&o
(PELD– CNPq) - Sitio 04. Available from: &&&&&&&&[  ]BYSTR&OM, P., KARLSSON, J., NILSSON, P.,
VAN KOOTEN, T., ASK, J. and OLOFSSON, F., 2007. Substitution of top predators:
effects of pike invasion in a subarctic lake. Fresh. Biol., vol. 52,
no. 7, p. 0.
&&&&&&&&[  ]
CARPENTER, SR., KITCHELL, JE. and HODGSON, JR.,
1985. Cascading trophic interactions and lake productivity. BioScience,
vol. 35, no. 10, p. 634-639.
&&&&&&&&[  ]
CNPQ / PELD – SITE 4, 2007. Mata Atl&ntica
e Sistema Lacustre do M&dio Rio Doce. Pesquisas Ecol&gicas de
Longa Dura&&o – S&tio No 4. Available from: .
&&&&&&&&[  ]
COX, GW. and RICKLEFS, RE., 1977. Species diversity,
ecological release, and community structuring in Caribbean land bird faunas.
Oikos, vol. 29, no.1, p. 60-66.
&&&&&&&&[  ]
DE MELO, R., FRANCE, R. and MCQUEEN, DJ., 1992.
Biomanipulation: Hit or Myth? Limnol. Oceanogr., vol. 37, no.1, p. 192-207.
&&&&&&&&[  ]
FAPEMIG/Rio Doce, 2007. Biblioteca digital
dos recursos h&dricos do m&dio rio Doce. Minas Gerais: Funda&&o
de Amparo & Pesquisa de Minas Gerais, FAPEMIG. Available from: .
&&&&&&&&[  ]
FERNANDO, CH. 1994. Zooplankton, fish and fisheries
in tropical freshwaters. Hydrobiologia, vol. 272, no. 1-3, p. 105-123.
&&&&&&&&[  ]
GLIWICZ, MZ., 1986. Predation and the evolution
of vertical migration in zooplankton. Nature, vol. 320, no. 6064, p.
746-748.
&&&&&&&&[  ]
GODINHO, AL., FONSECA, MT. and ARA&UJO,
ML., 1994. The ecology of predator fish introductions: the case of rio Doce
valley lakes. In PINTO-COELHO, RM., GIANI, A. and VON SPERLING, E. (Eds.). Ecology
and human impact on lakes and reservoirs in Minas Gerais with special reference
to future development and management strategies. Belo Horizonte: SEGRAC.
p. 77-83.
&&&&&&&&[  ]
GODINHO, AL. and FORMAGIO, PS., 1992. Efeitos
da introdu&&o de Cichla ocellaris e Pygocentrus
sp. sobre a comunidade de peixes da Lagoa Dom Helv&cio. Encontro Anual
de Aq&icultura de Minas Gerais, vol. 10, p. 93-102.
&&&&&&&&[  ]
GODINHO, AL. and VIEIRA, F., 1998. Ictiofauna.
In COSTA, C. (Ed.). Biodiversidade em Minas Gerais: Um atlas para sua
conserva&&o. Belo Horizonte: Funda&&o Biodiversitas.
p. 44-46.
&&&&&&&&[  ]
GOTELLI, NJ. and ENTSMINGER, GL., 2001. EcoSim:
Null models software for ecology. Version 7.0. Acquired Intelligence Inc. &
Kesey-Bear. Available from: .
&&&&&&&&[  ]
GUIMAR&AES, AS., AOKI, A., VALADARES, CF.,
MELLO, NAST., PEIXOTO, RS., MENENDEZ, RM., BRAZ, AS., BRITO, SL. and MAIA-BARBOSA,
PM., 2005. Comunidade zooplanct&nica de sete lagos do Parque Estadual
do rio Doce e entorno. In BARBOSA, FAR. (Coord.). Relat&rio T&cnico-Cient&fico
das atividades de janeiro a dezembro 2005 - Pesquisas Ecol&gicas de Longa
Dura&&o (PELD–CNPq) - Sitio 04. Available from: &&&&&&&&[  ]JEPPESEN, E., MEERHOFF, M., JACOBSEN, BA., HANSEN,
RS., S&ONDERGAARD, M., JENSEN, JP., LAURIDSEN, TL., MAZZEO, N. and BRANCO,
CWC., 2007. Restoration of shallow lakes by nutrient control and biomanipulation
— the successful strategy varies with lake size and climate. Hydrobiologia,
vol. 581, no. 1, p. 269-285.
&&&&&&&&[  ]
KAUFMAN, L., 1992. Catastrophic change in species-rich
freshwater ecosystems: the lessons of Lake Victoria. Bioscience, vol.
42, no. 11, p. 846-858.
&&&&&&&&[  ]
LATINI, AO., PEREIRA, TL., LATINI, RO., GIACOMINI,
HC., LIMA J&UNIOR, DP., OPORTO, LT. and ESP&IRITOSANTO, HMV., 2005.
Distribui&&o e efeitos de peixes ex&ticos sobre a ictiofauna
nativa dos lagos do M&dio Rio Doce, MG, Brasil. In ROCHA, O., ESP&INDOLA,
E., VERANI, N., VERANI, JR., RIETZLER, AC. (Eds.). Esp&cies invasoras
em &guas doces: estudos de caso e propostas de manejo. 1 ed. S&o
Carlos, SP: Gr&fica Expressa. p. 99-129.
&&&&&&&&[  ]
LATINI, AO. and PETRERE, M., 2004. Reduction
of native fish fauna by alien species: an example from Brazilian freshwater
tropical lakes. Fish. Manag. Ecol., vol. 11, no. 2, p. 71-79.
&&&&&&&&[  ]
LEWIS, W., 2000. Basis for the protection and
management of tropical lakes. Lakes Reserv.: Res. Manage., vol. 5, no.
1, p. 35-48.
&&&&&&&&[  ]
LORENZEN, CJ., 1967. Determination of chlorophyll
and pheopigments: spectrophotometric equations. Limnol. Oceanogr., vol.
12, no. 2, p. 343-346.
&&&&&&&&[  ]
LOSOS, JB. and QUEIROZ, K., 1997. Evolutionary
consequences of ecological release in Caribbean Anolis lizards. Biol. J.
Linn. Soc., vol. 61, no. 4, p. 459-483.
&&&&&&&&[  ]
MAIA-BARBOSA, PM., MENENDEZ, RM., VALADARES,
CF., BRAND&AO, ECL., BRAZ, AS. and BRITO, SL., 2003. Composi&&o
da comunidade zooplanct&nica de rios e lagos do trecho m&dio da
bacia do Rio Doce-MG. In BARBOSA, FAR. (Coord.). Relat&rio T&cnico-Cient&fico
das atividades de agosto 2002 a dezembro - Pesquisas Ecol&gicas de Longa
Dura&&o (PELD– CNPq) - Sitio 04. Available from: &&&&&&&&[  ]MAIA-BARBOSA, PM., MENENDEZ, RM., VALADARES,
CF., BRAND&AO, ECL., BRAZ, AS., BRITO, SL., AOKI, A. and MELLO, NAST.,
2004. Composi&&o da comunidade zooplanct&nica de rios e
lagos do trecho m&dio da Bacia do Rio Doce-MG. In: BARBOSA, FAR. (Coord.).
Relat&rio T&cnico-Cient&fico das atividades de janeiro
a dezembro 2004 - Pesquisas Ecol&gicas de Longa Dura&&o
(PELD– CNPq) - Sitio 04. Available from: &&&&&&&&[  ]MATSUMURA-TUNDISI, T. 1997. Composition and vertical
distribution of zooplankton in Lake Dom Helv&cio. In TUNDISI, JG. and
SAIJO, Y. (Eds.). Limnological studies on the Rio Doce Valley Lakes, Brazil.
Brazilian Academy of S University of S&o Paulo, School of Engineering
at S&o Carlos, Center for Water Resources and Applied Ecology. p. 266-274.
&&&&&&&&[  ]
MATSUMURA-TUNDISI, T. and TUNDISI, JG., 1986.
Biomass and zooplankton comunity struture of three lakes of river Doce Valley
(MG-Brazil). In WATANABE S. (Org.). Fifth Japan-Brazil Symposium on Science
and Technology (Supplement). Tokyo: Japan. p. 35-43.
&&&&&&&&[  ]
MORETO, EM., 2001. Diversidade zooplanct&nica
e vari&veis limnol&gicas das regi&es limn&tica e
litor&nea de cinco lagoas do Vale do Rio Doce-MG, e suas rela&&es
com o entorno. S&o Carlos: Universidade Federal do S&o Carlos
– UFSCar. 310 p. [Master Dissertation]
&&&&&&&&[  ].
PINTO-COELHO, RM., PINEL-ALLOUL, B., M&ETHOT,
G. and HAVENS, K., 2005. Crustacean zooplankton in lakes and reservoirs of temperate
and tropical regions: variations with trophic status. Can. J. Fish. Aquat.
Sci., vol. 61, no. 2, p. 348-361.
&&&&&&&&[  ]
RICCIARDI, A., 2003. Predicting the impacts of
an introduced species from its invasion history: an empirical approach applied
to zebra mussel invasions. Fresh. Biol., vol. 48, no. 6, p. 972-981.
&&&&&&&&[  ]
ROCHA, O. and MATSUMURA-TUNDISI, T., 1997. Respiration
rates of zooplankton community of epilimnion and metalimnion layers of Lake
Dom Helv&cio during stratified and overturn periods. In: TUNDISI, JG.
and SAIJO, Y. (Eds.). Limnological Studies on the Rio Doce Valley Lakes,
Brazil. Brazilian Academy of S University of S&o Paulo, School
of Engineering at S&o Carlos, Center for Water Resources and Applied
Ecology. p. 286-296.
&&&&&&&&[  ]
SANTOS, LC., 1980. Estudos das popula&&es
de Cladocera em cinco lagos naturais (Parque Estadual do Rio Doce) que se encontram
em diferentes est&gios de evolu&&o. S&o Carlos:
Universidade Federal de S&o Carlos. 260 p. [Master Dissertation]
&&&&&&&&[  ].
SIMON, KS. and TOWNSEND, CR., 2003. Impacts of
freshwater invaders at different levels of ecological organisation, with emphasis
on salmonids and ecosystem consequences. Fresh. Biol., vol. 48, no. 6,
p. 982-994.
&&&&&&&&[  ]
SOTO, D., ARISMENDI, I., GONZ&ALEZ, J.,
SANZANA, J., JARA, F., JARA, C., GUZMAN, E. and LARA, A., 2006. Southern Chile,
trout and salmon country: invasion patterns and threats for native species.
Rev. Chil. Hist. Nat., vol. 79, no. 1, p. 97-117.
&&&&&&&&[  ]
TUNDISI, JG., MATSUMURA-TUNDISI, T., FUKUARA,
H., MITAMURA, O., GUILL&EN, SM., HENRY, R., CALIJURI, MC., IBA&NEZ,
MSR., ESP&INDOLA, ELG. and GOVONI, S., 1997. Limnology of fifteen lakes.
In TUNDISI, JG. and SAIJO, Y. (Eds.). Limnological studies on the Rio Doce
Valley Lakes, Brazil. Brazilian Academy of S University of S&o
Paulo, School of Engineering at S&o Carlos, Center for Water Resources
and Applied Ecology. p. 409-439.
&&&&&&&&[  ]
UTERM&OHL, H., 1958. Perfeccionamento del
metodo cuantitativo del fitoplancton. Commun. Assoc. Int. Limnol. Theor.
Appl., vol. 9, no. 1, p. 1-89.
&&&&&&&&[  ]
WISSEL, B., FREIER, K., MULLER, B., KOOP, J.
and BENDORF, J., 2000. Moderate planktivorous fish biomass stabilizes biomanipulation
by suppressing large invertebrate predators of Daphnia. Arch. Hydrobiol.,
vol. 149, no. 2, p. 177-192.
&&&&&&&&[  ]
Received October 9, 2007
Accepted October 9, 2007
Distributed November 30, 2008
e-mail:
All the contents of this journal, except where otherwise noted, is licensed under a