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Gill parasites of fish and their relation to host
and environmental factors in two estuaries in northeastern
Brazil
Julia M. Falkenberg .Je
´ssica Emı
´lia S. A. Golzio .Andre
´Pessanha .
Joana Patrı
´cio .Ana L. Vendel .Ana C. F. Lacerda
Received: 10 September 2018 / Accepted: 16 January 2019
ÓSpringer Nature B.V. 2019
Abstract Fish parasites can be good indicators of the
quality of water bodies, and their presence or absence
can be interpreted as a sign of habitat changes, helping
us to diagnose environmental problems. This study
was conducted in two estuaries located in the Paraı
´ba
state, northeastern Brazil: Mamanguape, an environ-
mental protection area, and Paraı
´ba do Norte, a river
with riverside communities along its length. The
objective of the study was to determine whether host
and abiotic characteristics predict the richness of fish
gill parasites and/or the abundance of the most
abundant and prevalent parasite species, the copepod
Acusicola brasiliensis, testing the species as a possible
bioindicator. The fish host species were Anchoa
januaria,Atherinella brasiliensis,Mugil curema, and
Rhinosardinia bahiensis. Generalized linear models
were constructed to test the influence of predictor
variables on parasite richness and A. brasiliensis
abundance. The predictor variables used in the models
were the host relative condition factor (Kn), host
length, collection season (rainy or dry), estuary, host
species, total phosphorus, and chlorophyll a. Both
Handling Editor: Te
´lesphore Sime-Ngando.
J. M. Falkenberg A. C. F. Lacerda
Laboratory of Hydrology, Microbiology and Parasitology,
Federal University of Paraı
´ba, Joa
˜o Pessoa, PB, Brazil
J. M. Falkenberg
Graduate Program in Ecology and Environmental
Monitoring, Federal University of Paraı
´ba, Joa
˜o Pessoa,
PB, Brazil
J. E. S. A. Golzio A. C. F. Lacerda
Graduate Program in Zoology (Biological Sciences),
Federal University of Paraı
´ba, Joa
˜o Pessoa, PB, Brazil
A. Pessanha
Graduate Program in Ecology and Conservation, State
University of Paraı
´ba, Campina Grande, PB, Brazil
J. Patrı
´cio
Faculty of Sciences and Technology, MARE-Marine and
Environmental Sciences Centre, University of Coimbra,
Coimbra, Portugal
A. L. Vendel
State University of Paraı
´ba - Campus V, Joa
˜o Pessoa, PB,
Brazil
J. M. Falkenberg (&)
Departamento de Sistema
´tica e Ecologia, Universidade
Federal da Paraı
´ba, Cidade Universita
´ria, s/n,
58051-900 Joa
˜o Pessoa, PB, Brazil
e-mail: falkenbergjulia1@gmail.com
123
Aquat Ecol
https://doi.org/10.1007/s10452-019-09676-6(0123456789().,-volV)(0123456789().,-volV)
parasite species richness and A. brasiliensis mean
abundance showed a significant relation to water
quality parameters, suggesting their possible use as
environmental quality indicators.
Keywords Ichthyoparasitology Ectoparasites
Bioindicators Water pollution
Introduction
The parasites of aquatic organisms are intrinsically
related to various habitat characteristics (Lafferty and
Kuris 1999). Due to their diversified life cycles, these
organisms may be susceptible to changes in the
environment, responding with an increase or a
decrease in abundance and diversity (Marcogliese
and Cone 1997; Marcogliese 2005). For this reason,
parasites have attracted researchers’ interest as poten-
tial indicators of environmental quality due to the
variety of forms that respond to anthropic pollution,
such as oil spills; heavy metals; eutrophication; acid
precipitation; and household, agricultural, and indus-
trial sewage (Landsberg et al. 1998; Sures 2004).
However, the parasite fauna in many systems remains
unknown, regardless of whether the systems are
healthy or affected by different anthropogenic
impacts. With the imbalance in the biotic integrity of
the aquatic ecosystem, changes in the community of
parasites may reflect the loss of environmental quality
(Lafferty 1997).
Like free-living species, parasites respond to dis-
turbances in the ecosystem and can provide valuable
information about the quality, integrity, and health of
systems in response to pollutants and other stressors
(Sures et al. 2017). Parasitic taxa can respond differ-
ently to different types of pollution (Lafferty 1997). As
an example, ciliates and nematodes are sensitive
indicators of eutrophication (Palm and Dobberstein
1999), and digeneans and acanthocephalans are sen-
sitive indicators of heavy metals and anthropogenic
disturbances (Jeney et al. 2002; Billiard and Khan
2003; Sures 2003). The quality of the water and the
substrate is fundamental for the maintenance of
organisms at the base of the trophic chains, as well
as of the fish in their initial ontogenetic stages, which
are particularly more susceptible to environmental
imbalances and mortality (Marcelino et al. 2005).
According to Galli et al. (2001), the fish parasite
community should be used as an indicator of water
quality because parasites are more abundant than their
hosts, many fish parasites require invertebrates to
complete their cycles (thus parasites reflect changes in
aquatic invertebrate communities), and parasites move
through the trophic web and are at the top of the
trophic web, integrating the adverse effects of the
different contaminants.
Considering the increasing impacts of anthro-
pogenic origin on the Paraı
´ba estuaries in the Brazilian
state of Paraı
´ba, the estuaries of Paraı
´ba do Norte
(RPN) and Mamanguape (RMA) Rivers provide an
excellent opportunity to study parasites as environ-
mental indicators. Paraı
´ba do Norte River is contin-
uously impacted by anthropogenic activities, causing
direct and indirect interference in the behavior and
biological cycle of several species in the area
(Watanabe et al. 1994), whereas Mamanguape River
is located in an environmental protection area (EPA)
(Paludo and Klonowski 1999), which is expected to be
less impacted. Alves et al. (2016) performed a detailed
characterization of these two estuaries and their water
variables, observing that the main differences between
them were related to nutrient concentrations (total P,
NH
3
–N, and NO
x
–N), which were generally much
higher in the RPN than in the RMA, independent of
zone or season, reflecting the higher degree of
anthropogenic disturbance in the RPN. Aquatic organ-
isms are exposed to a number of natural or anthro-
pogenic stressors, such as variations in the physical
and chemical parameters (rainfall and temperature),
changes in habitat and food availability, exposure to
contaminants, and increased nutrient supply (eutroph-
ication) (Catalano et al. 2014). The fish parasites may
reflect the environmental quality and the host habitats,
and the parasites may interact with different levels of
microorganism and fish community structures, con-
stituting potential bioindicators for the study region
(Machado 1999; Adams and Greeley 2000). Recently,
Golzio et al. (2017) published the first survey on fish
parasites from the estuaries RPN and RMA, recording
eighteen species of parasites, but no studies have
reported on the ecological aspects of fish parasites for
these two estuaries.
Considering the importance of understanding and
contributing with improvements in the management of
estuarine environments, the expansion of fish parasite
studies is necessary for these environments to protect
123
Aquat Ecol
them from the impacts of anthropogenic pollution. So,
the objective of this study was to determine whether
host and water abiotic characteristics predict the
richness and mean abundance of fish gill parasites,
comparing the community of fish parasites of two
estuaries, one with high anthropogenic impact and
another in an EPA.
Materials and methods
Study area
Paraı
´ba do Norte River Estuary (ERP) covers the
municipalities of Santa Rita, Bayeux, Joao Pessoa,
Lucena, and Cabedelo and is located between latitudes
6°5401400 and 7°0703600S and the longitudes 34°5801600
and 34°4903100W (Fig. 1a). The estuary region has
typical characteristics of a river submitted to a
medium water flow regimen and is surrounded by
extensive plantations of sugarcane and shrimp farms
(Mace
ˆdo et al. 2017). The estuary is flanked by what
remains of the mangrove forest, which has been quite
altered due mainly to sugarcane plantations and urban
clusters (Marcelino et al. 2005), which are sources of
considerable anthropogenic impacts.
Mamanguape River Estuary (ERM) is located on
the northern coast of the state of Paraı
´ba at 6°4300200S
and 35°6704600W (Fig. 1b). It extends approximately
25 km east–west and 5 km north–south, constituting
an area of 16,400 ha that is part of EPA of Barra de
Mamanguape (CERHPB 2004). This estuary differs
from typical estuaries due to the 8.5-km reef line that
runs parallel to the shore at the mouth of the estuary,
creating a protected region with calm waters (Vendel
et al. 2017). This estuary occupies 690 ha, with well-
preserved mangroves around the main channel and
tidal creeks. For a detailed description of the two
estuaries, see Alves et al. (2016) and Dolbeth et al.
(2016).
Fig. 1 Paraı
´ba do Norte River Estuary (a) and Mamanguape River Estuary (b), Paraı
´ba state, Brazil. Collection points and land use
cover. Author: S. Vital
123
Aquat Ecol
The distance between the two estuaries is approx-
imately 22 km. The climate of the region is Ko
¨ppen
type As, hot and humid. According to data from the
AESA (2011), rainy season starts in February and lasts
until July, with maximum rainfall in April, May, and
June; dry season occurs in spring to summer, with
more severe drought in the months of October to
December. The normal annual precipitation is
between 1750 and 2000 mm annually, and the average
temperature is approximately 24–26 °C.
Water variables
Collections were conducted in November of 2013 (dry
season) and in July 2014 (rainy season) at the same
points, and sampling sites were defined along the two
estuaries (15 in the ERP and 12 in the ERM, Fig. 1).
The water clarity (m) was measured with a Secchi
disk. Surface values for salinity (ppm), water temper-
ature (°C), pH, turbidity (NTU), and total dissolved
solids (TDS; g/L) were measured in situ using a
multiparameter probe (Horiba/U-50). The concentra-
tions of ammonia (lg/L), nitrite (lg/L), and nitrate
(lg/L) (Apha 2005) and of total phosphorus (lg/L)
(Strickland and Parsons 1972) were measured in the
laboratory at the State University of Paraı
´ba
(UEPB)—Campus I. The concentration of chlorophyll
a(lg/L) was evaluated according to Lorenzen (1967).
Fish
In each season, three manual trawls were conducted
for an approximate extension of 30 m with a net
measuring 10 m long 91.5 m high, with 5-mm mesh.
In addition, during the dry season collection, three
series of 20 cast net throws were conducted at each
collection site. The weight and total length of each fish
were measured in the UEPB Laboratory, and the fish
was then fixed in formaldehyde. Subsequently, fish
necropsy and parasite collection, fixation, and preser-
vation were conducted at the Laboratory of Aquatic
Ecology (LABEA) and the Paulo Young Laboratory of
Invertebrates (LIPY), both at the Federal University of
Paraı
´ba. The host species analyzed were Atherinella
brasiliensis (Quoy and Gaimard 1825) (N= 407, 241
of dry season and 166 of wet season), Anchoa januaria
(Steindachner 1879) (N= 135, 67 of dry season and
68 of wet season), Mugil curema Valenciennes, 1836
(N= 214, 78 of dry season and 136 of wet season), and
Rhinosardinia bahiensis (Steindachner 1879)
(N= 36, only wet season).
Parasites
Fish were necropsied, and their gills were removed
and observed under a stereomicroscope. Then, gills
were stored in 70% ethanol. For identification of the
parasites, the specimens were clarified in Amman’s
lactophenol (Nematoda) or stained with Gomori
trichrome and mounted in Hoyer’s or Gray and Weiss’
medium (Monogenea) or stained with Carmine Acetic
(Digenea) or clarified and mounted in Hoyer’s or Gray
and Weiss’ medium (Copepoda). Subsequently, the
slides were mounted in Canada balsam for identifica-
tion with the aid of a microscope. Identification was
performed according to Travassos et al. (1969),
Moravec (1998), Gibson et al. (2002), and Thatcher
(2006). Values of prevalence, mean intensity, and
mean infection abundance and the ecological termi-
nology were determined according to Bush et al.
(1997).
Analyses
Two generalized linear models (GLMs) were con-
structed using the R programming environment (R
Core Team 2010). A model was constructed with
parasite richness (number of parasite species in a
single host) as the response variable, and another was
constructed by using the abundance of the most
prevalent and abundant parasite. In both models, the
following variables were tested as possible predictor
variables: estuary, collection season, region of the
estuary (upstream and downstream), water clarity,
TDS, nitrate, ammonia, total phosphorus, chlorophyll
a, host species, total host length, and host relative
condition factor. The relative condition factor (Kn)
was calculated according to Le Cren (1951), where the
expected weight and the observed weight are used to
calculate, which has a value equal to one (1) under
normal conditions. After the graphical analysis of the
residuals, the variables clarity, TDS, nitrate, and
ammonia were removed from the models because
they presented collinearity with the other variables.
The most appropriate models to explain variations in
the response variable were determined using backward
model selection and the Akaike information criterion,
where all the variables are initially included in the
123
Aquat Ecol
model, and the least significant variables are sequen-
tially removed from the model. Significant values
(\0.05) are considered an indication that variations in
the response variable can be explained by variations in
the predictor variable.
Results
The mean values of the environmental variables
during the rainy and dry season collections are shown
in Table 1. A total of 836 fish were analyzed, and fish
total length (in mm) and total mean size ±standard
deviation per species including for non-parasitized fish
(TT) and for the parasitized fish (TP) were as follows:
A. brasiliensis (TT = 51.6 ±29.2; TP = 91.5 ±
20.3), A. januaria (TT 54.8 ±13.3, TP = 61.8 ±
7.9), M. curema (TT = 39.8 ±36.4, TP = 55.1 ±
12.9), and R. bahiensis (TT = 59.1 ±6.1,
TP = 67.6 ±16.2).
Among the fish examined, 125 (preva-
lence = 20.3%) had gills parasitized by at least one
parasite species. Atherinella brasiliensis had the
highest number of individual fish parasitized (87),
followed by M. curema (18), A. januaria (15), and R.
bahiensis (5). In total, 18 parasite species were
recorded, belonging to the Monogenea (Ligophorus
mugilinus), Digenea (Parahemiurus merus and Rhipi-
docotyle sp.), Nematoda (Pharingodonidae gen. sp. 1
and Pharingodonidae gen. sp. 2), Copepoda (Acusi-
cola brasiliensis,Bomolochus xenomelanirisi,B.
nitidus, Caligidae gen. sp., Ergasilus sp, E. atafonen-
sis,E. bahiensis, and E. caraguatubensis), and Isopoda
(Artystone sp., Lironeca sp., Mothocya argenosa,
Mothocya nana, and Mothocya omidaptria) (see
Golzio et al. 2017 for a complete host–parasite
checklist and parasitism indexes). Parasite species
richness per host varied between 0 and 4 (0.2 ±0.3).
The copepod A. brasiliensis Amado and Rocha 1996
found in the gills of A. januaria and A. brasiliensis was
the most abundant and prevalent parasite (accounting
for more than 20% in both estuaries for the host A.
brasiliensis) and was therefore chosen for the con-
struction of the models.
Predictive variables retained in each model are in
Table 2. The lowest richness was found in ERP and in
the species M. curema. In the models using the
abundance of the copepod A. brasiliensis as the
response variable, the highest parasite abundance
values were in ERM and in the upstream region of the
estuary.
Discussion
Fish parasites are susceptible to intrinsic (host-related)
and extrinsic (environment-related) factors (Dogiel
1961). In this context, the identification of correlations
among parasitism, environmental variables related to
productivity, and host characteristics was possible.
Parasite species richness was significantly lower in
the ERP, the most polluted study area. According to
Marcogliese (2005), parasites are a natural part of
ecosystems, and healthy ecosystems must present a
healthy parasite community. A healthy ecosystem
(functional and resilient) is a system rich in parasitic
species (Costanza and Mageau 1999) because, as the
free-living species, parasites respond to disturbances
and can provide important information about the
quality, integrity, and health of the ecosystem in
Table 1 Mean ±standard deviation of the environmental variables sampled in the estuaries of the Paraı
´ba do Norte (ERP) and
Mamanguape (ERM) Rivers in the dry season (November 2013) and rainy season (July 2014)
ERP ERM
Dry Rainy Dry Rainy
Clarity (m) 0.7 ±0.2 0.8 ±0.2 0.9 ±0.3 0.8 ±0.2
TDS (g/L) 13.8 ±9.9 13.7 ±9.2 12.9 ±10.6 15.9 ±10.1
Nitrate (g/L) 259.9 ±756.7 231.8 ±2598.1 133.2 ±899.9 22.8 ±14.2
Ammonia (lg/L) 1020.3 ±951.9 2566.7 ±1353.1 182.2 ±393.9 1124.5 ±1624.6
Total phosphorous (lg/L) 598.8 ±153.3 510.3 ±234.2 299.7 ±138.7 236.1 ±171.1
Chlorophyll a (lg/L) 33.1 ±211.5 3.1 ±2.6 62.1 ±305.3 2.9 ±1.8
123
Aquat Ecol
response to pollutants and other stressors (Sures et al.
2017). Thus, our results corroborate the findings of
other authors (Dus
ˇek et al. 1998; Galli et al. 2001;
Williams and Mackenzie 2003; Madanire-Moyo and
Barson 2010; Alves et al. 2016), where more species
richness was also found in less polluted environments.
The lowest abundance of the copepod A. brasiliensis
was found in ERP, suggesting that the abundance of
these parasites is influenced by environmental factors
(Al-Niaeem et al. 2015). Ectoparasites such as cope-
pods are in constant contact with water and can,
therefore, experience any direct negative effects of a
pollutant, so the poor water quality may affect their
abundance, diversity, and reproduction (Pietrock and
Marcogliese 2003) or populations because pollutants
in the water also alter the host’s immune response
pattern (Mackenzie et al. 1995; Mackenzie 1999).
By examining the relative contribution of each
environmental variable, we have discovered that the
total phosphorus correlated positively to parasite
richness and abundance of A. brasiliensis. The
concentration of phosphorus in water is not considered
directly toxic to animals (Amdur et al. 1991);
however, phosphorus may present indirect toxicity
because phosphorus pollution is the main stimulus for
toxic algal blooms or anoxic conditions in water
(Carpenter et al. 1998). Chlorophyll a, a more direct
estimate of the presence of algae in the aquatic body,
showed a negative correlation both with the parasite
species richness and with the abundance of A.
brasiliensis. Chlorophyll a is usually linked to pro-
cesses of eutrophication in which compounds are
released from the photosynthesis of bacteria and algae
(Sarvala et al. 1998). Eutrophication is caused by high
levels of nutrients in aquatic systems, particularly
phosphorus and nitrogen, and is associated with
increased primary productivity, decreased clarity,
and the level of dissolved oxygen in water (Smith
1998; Bennett et al. 2001). Eutrophication sometimes
favors parasitism in aquatic systems (Valtonen et al.
1997; Lafferty and Kuris 1999; Vidal-Martı
´nez et al.
2010). This is due to increased productivity, thus
increasing the abundance of intermediate and/or
definitive hosts (Kennedy and Watt 1994). However,
in sites with higher nutrient inputs, toxic effects may
occur, and parasitism may decline, as well as available
hosts (Overstreet and Howse 1977). A consensus
exists that parasite response to pollution varies, among
other factors, according to the parasite group and the
type of pollution (Lafferty and Kuris 1999; Sures
2004; Vidal-Martı
´nez et al. 2010; Vidal-Martı
´nez and
Wunderlich 2017). Our results corroborate, in part,
those found in the meta-analysis of Vidal-Martı
´nez
et al. (2010), where crustacean parasites showed a
negative interaction with eutrophication, and the
parasite community showed a positive interaction
with eutrophication.
For A. brasiliensis, the parameters that showed a
significant relation with the copepod were total
phosphorus and chlorophyll a. Phosphorus and nitro-
gen can be considered mainly responsible for the
primary productivity and eutrophication of the aquatic
environment (Lizama et al. 2007). The total phospho-
rus and chlorophyll a together in high concentrations
indicate environments that are in a state of eutroph-
ication (Madi and Ueda 2009) and that were determi-
nant for A. brasiliensis abundance, being ectoparasite
and with direct contact with the water, as well as its
hosts, would support this nutrient supply from water.
In the resident host, Atherinella brasiliensis, the
abundance of Acusicola brasiliensis was significantly
higher than in A. januaria, which is transient host. This
Table 2 Results of the two
GLMs performed with
parasite richness and
copepod (A. brasiliensis)
abundance as the response
variables
Predictors Richness Abundance of Acusicola brasiliensis
zpz p
Northern Paraiba Estuary -3.612 \0.001 -9.870 \0.001
Wet season – – 8.057 \0.001
Total phosphorus (lg/L) 2.151 0.031 9.034 \0.001
Chlorophyll a (lg/L) -5.060 \0.001 -3.382 \0.001
Host Anchoa januaria ––-5.694 \0.001
Host Mugil curema -3.602 \0.001 – –
Length (mm) 7.264 \0.001 17.855 \0.001
Relative condition factor 3.721 \0.001 5.570 \0.001
123
Aquat Ecol
fact may be related to the adaptation of the parasites to
an environment in which the host passes a stage of life
relative to a host that only completes its life cycle in
the estuaries.
The host species with the lowest parasite richness
was M. curema, which, due to not being an estuarine
resident (Carvalho et al. 2007), withstands salinity
variation in order to use the estuarine area. This factor,
coupled with the season in which the hosts were
captured, possibly influenced the parasitic richness
because parasites would have to withstand daily
variation in salinity (Williams 1998). Acusicola
brasiliensis was found in a resident estuarine fish, A.
brasiliensis (Pessanha et al. 2000), and was able to
withstand variations of daily salinity of the environ-
ment, thus being a possible water quality bioindicator.
In addition, estuarine resident hosts can suffer from the
cumulative effects of parasites because they spend
their entire life cycle in the estuary.
Total length and relative condition factor of the
hosts correlated positively with parasite species rich-
ness and the abundance of A. brasiliensis.We
emphasize that most of the individuals in the present
study were juveniles. According to Poulin et al.
(2011), the size of the host is an important factor
determining the parasite richness because the bigger
the surface, the greater the space to acquire new
parasites. Additionally, in larger individuals, the
availability of internal and external space for parasite
attachment also becomes larger. The size of the host,
when considered in relation to its age, is one of the
most important factors in the variation of the size of
the parasitic populations. Age causes a series of
changes in the biology of the fish, mainly in relation to
the trophic levels, thereby having direct repercussion
on the composition of the parasitic fauna, but mainly
for the parasites acquired through the trophic chain
(Dogiel et al. 1961), which is not the case of copepods.
A number of studies show evidence that the number of
parasites per host increases with fish length (Poulin
1996; Isaac et al. 2000; Guidelli et al. 2003), which can
be observed in studies with several families and fish
species (Poulin and Morand 2004).
The condition factor for fish is a measure or
quantitative indicator of well-being (Vazzoler 1996)
and can be used to measure the animal’s health status
(Brasil-Sato and Pavanelli 1999; Lizama et al. 2006).
The condition factor and the presence or abundance of
certain species of parasites are related variables
(Lemly 1980; Isaac et al. 2004). However, under
natural conditions, fish are infected by many species
that coexist and demonstrate interrelations; that is,
each individual hosts a small community of parasites
(Bush et al. 1997). Thus, one must also consider the
effect of these sets of species on host health (Vital et al.
2011). Lizama et al. (2006) observed positive relations
between relative condition factor (Kn) and the abun-
dance of some parasite species in the host Prochilodus
lineatus, suggesting that larger fish with larger Kn
support relatively higher levels of parasitism. More-
over, parasites of low pathogenicity, as the copepods,
can occur in high abundance in the hosts, correlating
positively with their condition factor (Moreira et al.
2010). Additionally, hosts that acquire parasite resis-
tance due to adaptation may not have a negative
influence on the condition factor (Dias et al. 2004).
However, it is important to note that the models show
correlations that may or may not be a result of a cause–
effect relationship.
Overall, it has been possible to attest that both the
parasite richness and the abundance of the parasite A.
brasiliensis are related to the parameters that directly
reflect the pollution of water bodies. Studies using fish
parasites as bioindicators are increasing in number,
and good reviews (Lafferty 1997; Sures 2004; Vidal-
Martı
´nez et al. 2010; Sures et al. 2017) compile the
information generated, in an effort to suggest patterns
for using these organisms as indicators of water
quality. However, estuaries are understudied in this
aspect and deserve attention due to the peculiarities of
these environments. In addition, the challenge remains
in determining the responses of different groups of
parasites to various forms of pollutants and selecting
the best abiotic variables that reflect the environmental
conditions experienced by parasites, given the fact that
there are many interrelated variables, which hinders
their simultaneous use in models.
Acknowledgements The authors thank the Coordination of
Improvement of Higher Education Personnel (CAPES) for
financing the PVE/CAPES project (Process 173/2012) ‘‘What
lessons can be learned from ecological functioning in the
estuarine systems of the state of Paraiba? An analysis of the
effect of natural and anthropogenic disturbances’’ and the
Science without Borders Program (Special Visiting
Researcher). CAPES also funded J. Golzio through a master’s
scholarship. The National Council for Scientific and
Technological Development (CNPq) funded J. Falkenberg and
A. Coutinho through undergraduate scholarships (Scientific
Initiation). The authors thank Saulo Vital for the map.
123
Aquat Ecol
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