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Received: 10 March 2017
Revised: 24 July 2017
Accepted: 18 September 2017
DOI: 10.1002/rra.3225
Spatial and temporal distribution of ichthyoplankton during an
unusual period of low flow in a tributary of the São Francisco
River, Brazil
G.R. Rosa1
G.N. Salvador2
A. Bialetzki3
G.B. Santos1
Programa de Pós‐Graduação em Biologia de
Vertebrados, Pontifícia Universidade Católica
de Minas Gerais, Belo Horizonte, Minas Gerais,
Programa de Pós‐Graduação em Ecologia,
Universidade Federal do Pará, Belém, Pará,
Núcleo de Pesquisas em Limnologia,
Ictiologia e Aquicultura (Nupélia)/Programa de
Pós‐graduação em Ecologia de Ambientes
Aquáticos Continentais, Universidade Estadual
de Maringá, Maringá, Paraná, Brazil
G. R. Rosa, Programa de Pós‐Graduação em
Biologia de Vertebrados, Pontifícia
Universidade Católica de Minas Gerais. Av.
Dom José Gaspar, 500, prédio 41, 30535‐610,
Belo Horizonte, Minas Gerais, Brazil.
Email: [email protected]
Funding information
Companhia Energética de Minas Gerais
(CEMIG), Grant/Award Number: P&D GT‐
455; Coordenação de Aperfeiçoamento de
Pessoal de Ensino Superior (CAPES); Fundação
de Amparo a Pesquisa de Minas Gerais
(FAPEMIG), Grant/Award Number: APQ
Flow‐dependent fish specialists require specific conditions for reproduction, so the success and
reproductive intensity of these animals are determined by the flood regime. Thus, this
study investigated the spatial and temporal reproductive patterns of fish, especially migratory
Prochilodus species (flow‐dependent specialists) in an unusual period of low flow in the Pará River
sub‐basin, one of the main tributaries of the upper São Francisco River. For this, ichthyoplankton
collections were carried out between November 2013 and February 2014. Data were
analysed considering the spatial and temporal variations in density of eggs and larvae for
the upper, middle, and lower portions of the Pará River sub‐basin, and correlating this to
some environmental variables. The results showed that the small headwater stretch of the
Pará River is one relevant spawning area for migratory fish species. However, this area is isolated by the Cajuru reservoir, which makes it uncertain the recruitment of these embryos,
due to interruption of natural drift between spawning/nursery areas caused for reservoirs.
Larvae of newly hatched migratory species found in tributaries of the lower Pará River
sub‐basin also indicate these species use these tributaries as spawning grounds and migratory routes. The period in which the research was conducted represented the most atypical
low flow, one in the last 75 years, resulting in the low variability in the environmental parameters. Although few parameters increased briefly in this low flow period influenced by
greater rainfall in December, this precipitation was possibly responsible for the final gonadal
maturation and spawning of migratory species.
dams, eggs and larvae, migratory fish, Prochilodus, São Francisco river basin, spawning sites,
until February or March in some basins (Bialetzki et al., 1999;
Seasonal reproductive cycles are common to most freshwater fish
Hermes‐Silva, Reynalte‐Tataje, & Zaniboni‐Filho, 2009; Lopes,
species. These cycles are a result of evolutionary adjustments to
Garcia, Reynalte‐Tataje, Zaniboni‐Filho, & Nuñer, 2014; Reynalte‐
Tataje, Agostinho et al., 2012; Vazzoler, Suzuki, Marques, & Lizama,
(Jiménez‐Segura, Palacio, & Leite, 2010; Suzuki et al., 2009;
1997). During this period, high densities of ichthyoplankton are in
Vazzoler, 1966) and are strongly related to the availability of
drift (Araujo‐Lima & Oliveira, 1998; Araújo‐Lima, Silva, Petry,
resources for the offspring (Nikolski, 1978). For many species from
Oliveira, & Moura, 2001; Bialetzki, Nakatani, Sanches, Baumgartner,
tropical rivers, the reproductive cycle occurs annually during the
& Gomes, 2005; Corrêa, Hermes‐Silva, Reynalte‐Tataje, & Zaniboni‐
rainy season, which is generally marked by higher temperatures,
Filho, 2011; Reynalte‐Tataje, Nakatani, Fernandes, Agostinho, &
more specifically between October and January, but can extend
Bialetzki, 2011). In some rivers such as the Magdalena River, there
River Res Applic. 2017;1–14.
Copyright © 2017 John Wiley & Sons, Ltd.
are two reproductive seasons a year in response to the twice‐yearly
(P. argenteus) represents 50% of all catches from the Três Marias
flood seasons (Jiménez‐Segura et al., 2010).
reservoir located on the upper São Francisco River (Sato &
Every year in the Neotropical region, many species that perform
Godinho, 2003). Although they are commercially and ecologically
upstream migration when river levels rise release their fertilized eggs
important, information about the life history of these species, such
in the uppermost segments of the basin, and upon reaching the larval
as spawning, breeding period, and environmental variables that
stage, they drift into the marginal depressions (Espínola et al., 2014;
influence reproduction, is little known (Godinho & Kynard, 2006;
Gomes & Agostinho, 1997; Nakatani, Baumgartner, & Cavicchioli,
Sato, Bazzoli, Rizzo, Boschi, & Miranda, 2005; Sato & Godinho,
1997; Vazzoler, 1966). Thus, hydrology is a key factor to understand
2003). It is known that these species reproduce in the flood season
the inter‐annual variations in larvae assemblies (Cheshire, Ye,
between November and February with the release of hundreds of
Gillanders, & King, 2015), especially for the flow‐dependent specialist
thousands of eggs into the water column, coinciding with the rise
species (Baumgartner et al., 2014; Cheshire et al., 2015), which
in temperature and photoperiod, and that spawning probably
perform long‐distance migrations to spawn in response to increased
occurs on the bed of the main river and its tributaries (Bazzoli,
flow (Reynolds, 1983). Therefore, the reproductive success of many
2003; Santos et al., 2012; Sato, Cardoso, Godinho, & Godinho,
species is generally related to the flow regime, which has been touted
1996; Sato & Godinho, 2003).
as one of the main factors affecting spawning and fish recruitment
As there is a lack of knowledge relating to the life history of these
in large rivers (Agostinho, Gomes, Veríssimo, & Okada, 2004;
species, conducting studies of this is important to understand the
Humphries, King, & Koehn, 1999; Junk, Bayley, & Sparks, 1989;
reproductive dynamics of Neotropical fish assemblies (Gogola,
King, Humphries, & Lake, 2003).
Sanches, Gubiani, & Silva, 2013). Furthermore, these studies would
However, the present work was conducted in an atypical low flow
support much needed conservation and preservation projects of the
period, resulting in insufficient flooding to create lateral overflow of
Brazilian lotic remnants, since the use of hydroelectric energy,
the river. Under such conditions, would it be possible for some species
representing 64% of Brazil's total electricity production (Empresa de
to spawn and recruit? This possibility has been considered to the “low
Pesquisa Energética, 2016), is currently one of the largest threats to
flow recruitment hypothesis,” (LFRH), proposed by Humphries et al.
aquatic biodiversity due to habitat loss and fragmentation (Pelicice,
(1999). The main assumption of the LFRH, is that some species spawn
Pompeu, & Agostinho, 2015).
during the warmest months and lowest flows, state that species are
In addition to the impacts described above, hydroelectric plants
able to recruit under these conditions in a wide range of lentic and
also cause modifications to the hydrological regime, altering the
semi‐lentic environments along the major river (Humphries et al.,
entire dynamics of the floodplain and suppressing natural nurseries
1999). This hypothesis contradicts the widespread acceptance of the
upstream, which results in changes to the reproductive pattern of
importance of flooding and the flood plain for successful recruitment
migratory fish species (Agostinho, Pelicice, & Gomes, 2008). The
of the “flood pulse concept” proposed by Junk et al. (1989).
main changes are due to regulating the downstream frequency and
Depending on the regional characteristics of the basin during the
intensity of flood pulses that result from flow control, such as sedi-
breeding season, fish can use different stimuli and environments to
ment and nutrient retention and the quality of the released water
spawn (Humphries et al., 1999). This relationship between the
(Agostinho, Gomes, & Pelicice, 2007). Another significant impact is
environmental variables and ichthyoplankton distribution and abun-
the obstruction of the free passage of eggs and larvae through the
dance has been reported for several major Brazilian river basins. In
reservoirs, which has been identified as a major cause of population
the Paraná River basin, the occurrence of larvae increases mainly in
decline in migratory fish species (Agostinho, Gomes, & Pelicice,
periods of higher river levels and temperatures (Baumgartner et al.,
2007; Agostinho, Marques et al., 2007; Agostinho & Gomes, 1997)
2008; Baumgartner, Nakatani, Cavicchioli, & Baumgartner, 1997;
preventing the ichthyoplankton reaching the natural breeding sites
Castro et al., 2002), but pH and electrical conductivity possibly
located downstream (Pelicice et al., 2015; Suzuki, Zambaldi, &
induce some species to spawn, although this is still little known
Pompeu, 2013).
(Baumgartner et al., 2008). Similar patterns have also been reported
Thus, this study aimed to identify the areas and periods of fish
in the basins of the Uruguay (Corrêa et al., 2011; Hermes‐Silva
spawning, especially migratory species from the Prochilodus genus,
et al., 2009), Amazon (Oliveira & Ferreira, 2008), Magdalena
in a highly fragmented section, due to the presence of dams, of
(Jiménez‐Segura et al., 2010), and São Francisco Rivers (Sato &
the upper São Francisco River basin and detecting any environmental
Godinho, 2003).
variables related to the distribution and abundance patterns of the
In the São Francisco River basin, seven species are considered as
ichthyoplankton in an atypically dry period. For this, the following
long‐distance migratory ones, two of which, Prochilodus costatus
goals were proposed: (a) evaluate the spatial (sub‐basin stretches)
Valenciennes 1850 and Prochilodus argenteus Spix & Agassiz 1829,
and time distribution (sampling periods) of the ichthyoplankton
are abundant and endemic (Godinho & Kynard, 2006; Sato & Godinho,
during an unusual period of low flow; (b) identify possible spawning
2003). These species are benthopelagic, and therefore have an
areas for the migratory species of the Prochilodus genus based on
important ecological function in nutrient cycling (Castro & Vari,
sites with greater abundance of larvae in early developmental stages;
2003). In addition, species of the Prochilodus genus are greatly appreci-
and (c) verify the relationship between the physical–chemical (water
ated as fishing resources (Castro & Vari, 2003) because they are highly
abundant in the South American continental waters (Kerguelén‐
and hydrological variables (flow and rain) on the density of eggs
Durango & Atencio‐García, 2015). Alone, the Curimbatá‐pacu
and larvae.
W), Lambari River—LAM (19°31′50″S, 45°1′20″W), and Picão River
—PIC (19°18′23″S, 45°10′31″W). For the analyses, the sampling
stations were grouped into upper stretch (PA1, PA2, and ITA), middle
Study area
stretch (PA3, PA4, and SJO), and lower stretch (PA5, LAM, PEI, and
The study was conducted on the Pará River that has a drainage area
PIC), according to their position and contribution of the tributaries to
that is one of the most important contributors to the upper São
the respective sections of the main channel (Figure 1).
Francisco River basin in south‐eastern Brazil. The Pará River sub‐basin
has an area of approximately 12,500 km2 and water supplies around
38 municipalities with an approximate total population of 700,000
inhabitants. Located on the right bank of the upper São Francisco
River, the Pará River is the first upstream tributary after the Três
The ichthyoplankton samplings were carried out in two shifts, one in
Marias reservoir, and is in the south‐western portion of the state of
the evening (19:00–20:00) and one in the morning (06:00–07:00)
Minas Gerais. The river runs for approximately 365 km and its main
in order to avoid possible differences between day/night catches.
tributaries are the São João and Peixe Rivers, on the right bank, and
The ichthyoplankton was sampled fortnightly between mid‐November
the Itapecerica, Lambari, and Picão Rivers on the left bank (Comitê
2013 and February 2014, in the 10 stations, resulting in seven
de Bacia Hidrográfica do Rio Pará, 2006). The São João and Itapecerica
sampling periods (November 1; December 1; December 2; January 1;
Rivers are the ones most contaminated by sewage, with a water quality
January 2; February 1, and February 2). A conical–cylindrical plankton
index inadequate for public water supply, as well as being in regions
net (0.5 mm mesh, 0.12 m2 mouth area) was equipped with a General
crossing the most populous cities (Instituto Mineiro de Gestão das
Oceanics™ flow meter attached to the centre of the mouth to
Águas, 2014).
measure the volume of filtered water to enable standardization of
Dams for electricity generation are part of the overall picture of
the sampling effort.
the Pará River sub‐basin, making it highly fragmented. According to
During every shift, samplings lasting 10 min were conducted at the
the register of the Brazilian Electricity Regulatory Agency—ANEEL
same sampling stations, from the subsurface water of the central chan-
(, there are 14 medium‐ and
nel of the river. The samples were fixed in 4% formaldehyde solution,
small‐sized dams (Table 1) in the Pará River sub‐basin. The Pará and
buffered with calcium carbonate. In the laboratory, the eggs and fish
São João Rivers have the majority as well as the largest hydroelectric
larvae were separated from the sediment and then quantified using a
plants, while the Peixe and Picão Rivers are the only ones
stereoscopic microscope at 10× magnification. Larvae were identified
without dams.
using the reverse development sequence technique, as suggested by
Ten sampling stations were selected in the Pará River drainage
Ahlstrom and Moser (1976) and adapted by Nakatani et al. (2001),
basin, five of which were located in the main river: PA1 (20°24′19″S,
using body shape, presence of barbels, fin formation sequence,
44°37′41″W), PA2 (19°59′27″S, 44°53′51″W), PA3 (19°45′44″S,
position of the anal opening in relation to the body, the number of
44°53′57″W), PA4 (19°41′40″S, 44°55′47″W), and PA5 (19°16′38″
vertebrae/myomers, and fin radii. The taxonomic classification was
S, 45°7′51″W), and the other five in each the main tributaries:
made according to Britski, Sato, and Rosa (1988), Britski, Silimon, and
Itapecerica River—ITA (20°9′4″S, 44°53′23″W), São João River—SJO
Lopes (2007), Reis, Kullander, and Ferraris (2003), Graça and Pavanelli
(19°44′40″S, 44°49′7″W), Peixe River—PEI (19°27′21″S, 44°56′33″
(2007). Those identified as migratory species belonging to the genus
Small‐ and medium‐size hydroelectric plants in the Pará River sub‐basin
Reservoir length (km)
Reservoir area (km2)
Start of operation
Fish pass
Cachoeira Bento Lopes
Fish ladder
São João
São João
Coronel João Serqueira Lima
São João
Coronel Jove Soares Nogueira
São João
Dr Augusto Gonçalves
São João
São João
Retiro do Indaiá
João de Deus
Note. The data quoted was sourced from the ANEEL website (Brazilian Electricity Regulatory Agency; and from the literature and
hydroelectric companies' websites. Missing information was obtained by taking measurements using path tools and polygons available in Google Earth Pro
software to estimate the areas and lengths of the reservoirs. (Absent information:—).
Map of the Pará River sub‐basin with the ichthyoplankton collection stations subdivided into upper, middle, and lower stretches. Upper
—Pará River (PA1 and PA2) and Itapecerica River (ITA); middle—Pará River (PA3 and PA4) and São João River (SJO); lower—Pará River (PA5),
Lambari River (LAM), Peixe River (PEI), and Picão River (PIC)
Prochilodus and family Anostomidae were classified according to their
Data analysis
developmental stage according to Nakatani et al. (2001).
The environmental variables were measured simultaneously to
The abundance of organisms captured was standardized to a volume of
the ichthyoplankton collections using a YSI 556 MPS multiparameter
10 m3 of filtered water according to Tanaka (1973), modified by
probe, and data relating to temperature (°C), electric conductivity
Nakatani et al. (2001). In order to check the spatial distribution of the
(mS/cm), TDS (g/L), and pH were recorded. The streamflow (flow)
ichthyoplankton, the density of eggs and larvae resulting from each
and rainfall data were obtained from the Hidroweb website (National
replicate collected in different shifts were grouped by sampling station
Water Agency; and from the Minas
and these were categorized into sections (upper, middle, and lower).
Gerais Energy Company. The flow and rain gauge stations were
For the analysis of the temporal distribution, the densities resulting
selected considering the presence of tributaries and proximity to
from all shifts and sampling stations were grouped into sampling
the sampling station. The physical and chemical analyses of the PEI
periods. The Kruskal–Wallis test was used to evaluate spatial and tem-
sampling station were excluded due to the absence of current
poral variation (independent variables: basin section and sampling
streamflow data.
periods) in the eggs and larvae density (dependent variables). Where
Kruskal–Wallis results were significant, a Mann–Whitney test was
used a posteriori to detect these differences in basin section, as well
as in sampling periods.
For each sampling station, identified larvae densities (taxon/
10 m3) were obtained by summing each of the taxa collected considering all replicates, periods, and shifts. From these densities, the amount
of Prochilodus larvae in early development stages was determined for
each stretch, thereby identifying the proximity to its spawning areas
in the Pará River sub‐basin.
A principal component analysis (PCA) was performed with the aim
of summarizing environmental variables dimensionality in few axis. For
this analysis, all environmental variables except pH were transformed
into log (x + 1). The axes with eigenvalues greater than 1.0 were
retained for interpretation, according to the Kaiser–Guttman criterion
(Jackson, 1993). Variables with eigenvalues (correlations) greater than
0.4 were considered biologically important (Hair, Anderson, Tatham,
& Grablowski, 1984). In order to check the degree of association
between the density of eggs and larvae and the environmental
variables, a Spearman correlation between the scores of the retained
axes and the egg and larvae densities (eggs and larvae/10 m3) was
performed for each sampling station.
Average density (±standard error) of eggs/10 m3 (a) and
larvae/10 m3 (b) of fish from the different sampling stations,
subdivided into upper, middle, and lower stretches of the Pará River
(PA) sub‐basin, from November 2013 to February 2014
(marks = average; bars = standard error). ITA = Itapecerica River;
LAM = Lambari River; PEI = Peixe River; PIC = Picão River; SJO = São
João River
3.1 | Spatial and temporal distribution of the
A total of 6,540 eggs and 3,975 larvae were collected. It was only
possible to analyse the egg densities for the samples collected in the
December 1 period (representing 85.5% of the total density), due to
distribution of the eggs (Kruskal–Wallis test, H = 33.35, n = 420,
the lack of eggs found in the following periods. The densities were
p = .000) and larvae (Kruskal–Wallis test, H = 23.09, n = 420,
significantly different between the stretches, both for eggs (Kruskal–
p = .0008). For eggs and larvae, these significant differences occurred
Wallis test, H = 12.67, n = 60, p = .002) and larvae (Kruskal–Wallis test,
in December 1 and December 2 in relation to the other periods
H = 30.64, n = 420, p = .000).
(Mann–Whitney test; p < .05). The main reason for these peaks was an
The upper stretch of the studied sub‐basin had the highest density
increase of larvae density related to the reproductive peaks recorded
of eggs (2,703.6/10 m ), with the highest values in PA1 (mean x = 30.1,
in PIC (larvae) in December 2 and PA1 (eggs) in December 1. The high
standard deviation ± 92.5) and ITA (x = 0.9 ± 2.1; Figure 2a). The den-
density of eggs and larvae in December coincided with the period of
sities for this stretch were significantly higher than both the middle
the greatest flow in the Pará River sub‐basin.
stretch (Mann–Whitney test, U = 98.00, n = 36, p = .042), which exhibited the lowest density of eggs (40/10 m3), and the lower stretch
(Mann–Whitney test, U = 109.00, n = 46, p = .006), with an egg density
of 112.2/10 m3. Furthermore, small spawning peaks were recorded in
PEI (x = 1.8 ± 7.0) and PIC (x = 0.5 ± 2.4). Contrary to the egg density,
larvae density was highest in the lower portion of the sub‐basin (556/
10 m3), mainly due to the contribution of the tributaries, with the
highest densities found in PIC (x = 12.3 ± 36.7), PEI (x = 0.3 ± 0.8),
and LAM (x = 0.2 ± 0.3; Figure 2b). The density of larvae in the lower
portion of the Pará River sub‐basin was significantly higher than the
middle stretch (Mann–Whitney test, U = 7,742.00, n = 294, p = .000)
with a density of 15.7/10 m3 and to that of the upper stretch
(Mann–Whitney test, U = 8,047.50, n = 294, p = .000). The latter had
the lowest density of larvae (14.8/10 m3) in relation to other stretches.
December was the month with the greatest reproductive activity
of fish (Figure 3), which led to significant differences in the temporal
FIGURE 3 Distribution of eggs and larvae of fish over time
(mean ± standard error) in the Pará River sub‐basin between
November 2013 and February 2014 (marks = average; bars = standard
Larvae collected during the sampling period were distributed
Environmental variables
into four orders and 12 families (Table 2). The taxa with the
greatest abundance of larvae were Prochilodus, representing 57%
The greatest flow during the studied hydrological cycle occurred
of the total larvae density (107.7/10 m3), followed by Anostomidae
predominantly in December, but the hydrological cycle of 2013/
(8.3%, 16.1/10 m ), Triportheus guentheri (Garman 1890) (2.39%,
2014 in general can be categorized as a low flow cycle due to the
4.4/10 m ), and Serrasalmus brandtii Lütken 1875 (1.96%, 3.6/
low levels of rainfall that led to only a small increase in the river levels
10 m3). All larvae of Prochilodus and Anostomidae were in the yolk
in the region compared to previous hydrological cycles (Figure 5). The
larval stage. PIC was the site with the highest density of captured
average flow in the middle section of the Pará River between Novem-
Prochilodus larvae (105.3/10 m ; Figure 4). Only one Prochilodus
ber 2013 and February 2014 was 52 m3/s, the lowest average of the
larva was caught in the middle section of the sub‐basin (PA4), and
last 75 annual hydrological cycles for the same months (Figure 5a).
the remaining ones were captured only in the lower section (PEI,
The second lowest average of 62 m3/s occurred in the 1970/1971
LAM, PIC, and PA5). Among the larvae collected, 1,038 could not
hydrological cycle. Since 1938/1939 (the date the fluviometric station
be identified because they were either newly hatched or damaged.
utilized started operating), only another six annual hydrological cycles
However, most (955 larvae) were captured in the Picão River, when
presented a flow in the middle section less than 100 m3/s, ranging
the density peak of Prochilodus and Anostomidae larvae was regis-
from 100 to 288 m3/s in the other annual hydrological cycles. Because
tered. It is thus possible these unidentified larvae also belong to
of the unusual period of low flow, the measured environmental param-
these taxonomic groups.
eters varied little throughout the sampling period (Table 3). Therefore,
TABLE 2 Taxonomic groups and average densities of fish larvae by sampling station subdivided into the upper, middle, and lower stretches of the
Pará River sub‐basin
Mean larvae density (org/10 m3)
(Upper stretch)
(Middle stretch)
(Lower stretch)
Salminus hilarii
Piabarchus stramineus
Hoplias spp.
Prochilodus spp.
Myleus micans
Serrasalmus brandtii
Triportheus guentheri
Gymnotus carapo
Rhamdia quelen
Hypostomus spp.
Note. ITA = Itapecerica River; LAM = Lambari River; PA = Pará River; PEI = Peixe River; PIC = Picão River; SJO = São João River.
According to Reis et al. (2003), Britski et al. (2007), and Graça and Pavanelli (2007),
larvae identified to the order level;
larvae identified to the family level.
Density of larvae/10 m3 of the major taxonomic groups from each sampling station: Ano = Anostomidae; Bs = Piabarchus stramineus;
Cha = Characidae; Cic = Cichlidae; Gc = Gymnotus carapo; Hep = Heptapteridae; Hop = Hoplias spp.; Hyp = Hypostomus spp.; Lor = Loricariidae;
Mm = Myleus micans; Par = Parodontidae; Pim = Pimelodidade; Pro = Prochilodus spp.; Rq = Rhamdia quelen; Sb = Serrassalmus brandtii;
Sh = Salminus hilarii; Tg = Triportheus guentheri. ITA = Itapecerica River; LAM = Lambari River; PA = Pará River; PEI = Peixe River; PIC = Picão River;
SJO = São João River
the observed variations were mainly shaped by the characteristics of
Gomes, & Okada, 1993; Baumgartner et al., 2004; Vazzoler et al.,
each tributary and main riverbed stretch. Differences in environmental
1997). This happens because the upper regions have more inclined
variables that categorize the main river and its tributaries were
sections, providing efficient transportation of the organisms to the
observed, although the features of the upper Pará River stretches
embryonic development areas, particularly for migratory species
(PA1) resemble those of the tributaries.
(Baumgartner et al., 2004). The spawning site PA1 is located in a
Two PCA axes were retained for interpretation because they pre-
fragmented river stretch of approximately 65 km upstream of the
sented eigenvalues greater than 1.0 (Figure 6). The first one could
Cajuru reservoir. Successful spawning in small river fragments may
explain 65.9% of the variance while the second one represented
indicate that some populations of migratory species, such as the genus
19.9%, totalling 85.8% of the total variability. All variables were consid-
Prochilodus, do not require large stretches of river nor very specific
ered biologically important because they had eigenvalues greater than
conditions to spawn. Sporadic spawnings of migratory species were
0.40. Flow, temperature, conductivity, TDS, and pH were associated to
also observed in a stretch of less than 10 km between the Itá reservoir
the first axis (PCA1) and rainfall to the second one (PCA2). Significant
and the Machadinho dam in the Uruguay River (Reynalte‐Tataje,
correlations were obtained between egg density and the two axes of
Nuñer et al., 2012). Barzotto, Sanches, Bialetzki, Orvati, and Gomes
the PCA for PA1 (r = 0.60; p < .05), and between egg density and the
(2015) found indications that Prochilodus lineatus spawned in regions
PCA2 axis for PA5 (r = 0.55; p < .05). The larvae densities were signif-
where this activity is uncommon (drift areas), and they associated this
icantly correlated only to PCA1 for PA5 (r = 0.59; p < .05) and PIC
fact to the reproductive plasticity of this species, as has also been
(r = 0.84; p < .05).
observed in studies of its spawning resulting from hormonal induction
(Britski, 1972; Castro, 1993; Godoy, 1975). However, spawning does
not guarantee that recruitment will be successful, because it depends
on the availability of adequate environments for downstream larval
growth (Reynalte‐Tataje, Nuñer et al., 2012).
The highest density of eggs occurred in sampling station PA1, located
The low ichthyoplankton densities recorded in the sections down-
in the headwater of the main river, with many eggs from there having a
stream from the Gafanhoto and Cajuru plants suggest a discontinuity
wide perivitelline space, characteristic of migratory species according
of the natural drift process caused by the Cajuru reservoir. Impound-
to Nakatani et al. (2001). The longitudinal spatial pattern of
ment can change the downstream drift of particulate matter and biota
ichthyoplankton distribution, with a reducing number of eggs and
(Ward & Stanford, 1979; Ward & Stanford, 1995). Even small reser-
increasing number of larvae when going from upstream to down-
voirs may restrict the passive upstream to downstream displacement
stream, is known in many rivers and tributaries (Agostinho, Vazzoler,
of eggs and larvae produced by a population (Agostinho, Marques
FIGURE 5 Historical mean flow values and flow ranges from 76 consecutive hydrological cycles encompassing the months of November to
February obtained for the middle stretch of the Pará River (a). Daily flow (m3/s) of the Pará River (b) and its main tributaries: Itapecerica (c); São
João (d); Lambari (e); Picão (f) in flood regime periods (between November and February) for 10 consecutive hydrological cycles. The maximum flow
(dashed line) achieved during the hydrological cycle of this research (2013/2014) are also shown
et al., 2007; Pelicice et al., 2015). Such restrictions are related mainly to
result in genetic exchange. The passage of ichthyoplankton through
eggs and larvae predation due to the transparency of the water, mor-
reservoirs can be even more unlikely in atypical periods of low flow,
tality when passing through the turbines and spillways, slow displace-
as observed in this study. During these periods, there is a reduction
ment of the ichthyoplankton, or even deposition on the bottom of
of the useful volume of the reservoir, causing energy companies to
the reservoir where there are low oxygen concentrations and higher
restrict or even halt the spillage, so there is an increase in the residence
sedimentation rates (Agostinho, Gomes & Pelicice, 2007; Agostinho,
time of water. These changes in flow events are common in regulated
Marques et al., 2007; Pelicice et al., 2015). These events cause a deep
rivers, which can suffer changes in their magnitude, timing, duration,
effect on the genetic exchange for fish species with pelagic eggs
and variability (Ward & Stanford, 1979).
(Pelicice et al., 2015). The populations of P. costatus in the Pará River
Another change possibly linked to the Cajuru reservoir is the
are genetically distinct above, below, and between the Cajuru and
altered reproduction of fish downstream on the Pará River, because
Gafanhoto dams, a result of the migration interruption caused by their
the stretches after the reservoir showed low reproductive activity. This
construction more than six decades ago, and the constant fish stocking
result may be related to changes in the intensity, duration, and flood
programs, which have been carried out in the region for more than
periods caused by controlling the flow from the dam, generating unsta-
20 years (Barroca, Santos, Duarte, & Kalapothakis, 2012). This genetic
ble hydrodynamic conditions for downstream spawning (Godinho &
difference among P. costatus populations increases the likelihood there
Kynard, 2006; Sanches et al., 2006; Sato, Bazzoli, Rizzo, Boschi, &
is a discontinuity of the natural drift of ichthyoplankton caused by the
Miranda, 2003). These changes may also have boosted the use of the
Cajuru reservoir, as the passage from upstream to downstream should
lower Pará River tributaries as migratory routes, because the presence
25.87–29.83 ± 1.14
23.77–30.32 ± 1.89
23.91–25.77 ± 0.67
25.33 ± 29.04 ± 1.15
24.94–28.8 ± 1.06
23.66–26.66 ± 0.91
22.9–28.66 ± 1.89
25.31–29.22 ± 1.04
23.81–27.43 ± 1.01
Temperature (°C)
of dams contributes to the reduction of fish eggs and larvae in the main
river and hence, the use of tributaries as alternative migratory routes
(Hermes‐Silva et al., 2009).
The presence of larvae of newly hatched migratory species in tributaries indicates that these species use them as spawning grounds and
migratory routes (Barzotto et al., 2015; Gogola et al., 2013). Therefore,
the results of this study suggest that the tributaries of the lower Pará
for migratory species, considering the significant numbers of newly
0.07–0.12 ± 0.02
0.05–0.07 ± 0.01
0.08–0.24 ± 0.07
0.06–0.08 ± 0.01
0.07–0.13 ± 0.02
0.14–0.24 ± 0.03
hatched Prochilodus larvae recorded and the presence of the
0.04–0.05 ± 0
0.06–0.08 ± 0.01
0.06–0.09 ± 0.01
Conductivity (mS ± cm)
River, mainly the Peixe and Picão Rivers, are suitable spawning areas
Megaleporinus obtusidens (Valenciennes 1837) (Ávila‐Simas, Reynalte‐
Tataje, & Zaniboni‐Filho, 2014). Thus, as migratory larvae were only
captured at an early life stage, the Pará River sub‐basin could play an
important role as a spawning area (tributaries) and drift area
(main river). These larvae would be transported to downstream
possibly occurs.
There are a variety of temporary or permanent environments that
Note. ITA = Itapecerica River; LAM = Lambari River; PA = Pará River; PIC = Picão River; SJO = São João River; TDS = total dissolved solids.
7.19–8.94 ± 0.56
6.07–9 ± 0.85
8.51–9 ± 0.17
0–38.20 ± 11.61
0–31 ± 9.38
0–26.9 ± 9.91
42.5–167.76 ± 35.71
4.36–11.72 ± 2.53
1.6–3.84 ± 0.9
0.05–0.08 ± 0.01
0.03–0.05 ± 0
0.05–0.15 ± 0.04
6.7–8.84 ± 0.6
6.78–8.55 ± 0.52
6.27–8.62 ± 0.69
0–21.4 ± 6.93
0–22.7 ± 6.58
0–10.3 ± 3.26
28.68–69.58 ± 13.92
28.12–69.58 ± 14.66
7.71–9.19 ± 0.49
0.04–0.06 ± 0
0.05 ± 0.08 ± 0.01
0.09–0.16 ± 0.02
6.39–8.89 ± 0.82
6.85–8.82 ± 0.59
6.82–9.05 ± 0.66
0.03–0.03 ± 0
0.04–0.05 ± 0.01
0.04–0.06 ± 0.01
0–59.30 ± 20.96
0–22.2 ± 7.24
0–17.5 ± 4.68
9.93–13.92 ± 1.12
30.39–82.7 ± 15.53
5.46–38.86 ± 8.64
Sampling station
Flow (m3/s)
Rainfall (mm)
TDS (g/L)
areas, reaching the São Francisco River, where larval development
Range (minimum–maximum ± standard deviation) of environmental variables recorded at the sampled stations in the Pará River sub‐basin between November 2013 and February 2014
can be used for larval development such as marginal lagoons, canals,
floodplains, and river pools (Agostinho et al., 1993; Ávila‐Simas et al.,
2014; Humphries et al., 1999; King et al., 2003; Reynalte‐Tataje,
Hermes‐Silva, Silva, Bialetzki, & Zaniboni‐Filho, 2008; Scott & Nielsen,
1989). However, there are rivers or river stretches whose morphology
hinders the formation of these environments, such as the upper
Uruguay River that has steep slopes (Reynalte‐Tataje et al., 2008).
Similarly, in the 17 km stretch of the São Francisco River, between
the confluence of the Pará River and Três Marias reservoir, there are
few typical flood areas of the river such as floodplains and marginal
lagoons, as it only has a few areas of the river channel with low velocity
flow, such as river pools, backwaters, and marginal stretches. The scarcity of these areas plus the unusual period of low flow of this study
Principal component analysis (PCA) and the two retained
axes (PCA1 and PCA2) with eigenvalues (λ) greater than 1.0,
according to Kaiser–Guttman criteria (Jackson, 1993). All
environmental variables were represented on the axes because they
were considered biologically important with eigenvalues greater than
0.40, according to Hair et al. (1984). PCA1 axis explained 65.95% of
the variance, and PCA2 axis explained 19.96%. ITA = Itapecerica River;
LAM = Lambari River; PA = Pará River; PIC = Picão River; SJO = São
João River; TDS = total dissolved solids
brings into question the development of the larvae from the lower Pará
King et al., 2003), that, according to the LFRH (Humphries et al.,
River tributaries. The flood regime directly influences the survival rate
1999), may occur even in low flow conditions; (b) recruitment takes
during the early stages (Bailly, Agostinho, & Suzuki, 2008; Oliveira,
place in the regions of confluence of the tributaries and the main river,
Suzuki, Gomes, & Agostinho, 2015) and causes a deficit or even failure
which would be less likely in years of low flow because it would require
of migratory species recruitment in years when flooding is absent
significant floods to increase the water flow and restrain the water to
(Agostinho et al., 2008; Agostinho, Bonecker, & Gomes, 2009;
the lower parts of the tributaries and so facilitating the retention of
Fernandes et al., 2009), even when there is reproductive success in
the early stage larvae in suitable environments with low flow speed
the tributaries (Agostinho et al., 2008).
so they can perform activities such as feeding (Reynalte‐Tataje et al.,
Therefore, three patterns could explain the development and sur-
2008); and (c) failure in recruitment during periods of low flow,
vival of migratory larvae produced in the lower Pará River tributaries:
because the larvae would be exposed to predation after failing to reach
(a) recruitment in the bed of the São Francisco River in a mosaic of
potential sites for larval development during their early stages and,
diverse environments suitable for larval development, such as margins
therefore, remain drifting in the main river course (Agostinho et al.,
with low flow rate (Ávila‐Simas et al., 2014; Humphries et al., 1999;
2008). This would apply especially if they reach the Três Marias
Conceptual model of migratory species spawning based on the spatial results of this study, especially showing that the spawning areas
are predominantly in the lower Pará River tributaries
reservoir during their early stages, an environment unsuitable for larval
seek suitable environments for reproduction and larval development
development (Agostinho, Gomes, & Pelicice, 2007; Agostinho,
(Silva et al., 2014), and parameters such as conductivity and turbidity
Marques et al., 2007; Pelicice et al., 2015).
appear to be attractive for spawning, when they have high values
Spawning of Prochilodus was only registered in December in
(Agostinho, Marques et al., 2007).
different locations, coinciding with the only period of increased flow,
Based on these results, it is possible to summarize in a conceptual
suggesting a relationship between spawning and flow regime and the
model different elements related to the reproductive process of the
ephemerality of this phenomenon, because migratory species such as
migratory species from the Prochilodus genus in the Pará River
those from the Prochilodus genus produce numerous eggs that are
sub‐basin during a period of low flow (Figure 7). The dam‐free
released in a short time. These results agree with Agostinho and Júlio
tributaries of the lower stretch of the Pará River are noteworthy as
Júnior (1999) and Bazzoli (2003). In the Abaeté River, a tributary of
the environments responsible for maintaining Prochilodus fish stocks,
the São Francisco River, spawning of P. argenteus only happens during
as they offer spawning conditions even in atypical low flow periods,
the few days of flooding (Godinho & Kynard, 2006). Few species
such as the one in this study. Such environments are constantly threat-
reproduce throughout the year in the São Francisco River basin, and
ened by the increasing construction of small hydropower plants and
most of them show a spawning peak in December and January at the
medium‐size dams, very common in south‐eastern Brazil including
commencement of the flood season (Lamas, 1993). Unlike Prochilodus,
the Pará River sub‐basin that has at least 14 dams of this type. The
larvae of non‐migratory species, such as T. guentheri, S. brandtii,
Cajuru reservoir, located on the upper stretch of the Pará River, inter-
Piabarchus stramineus (Eigenmann 1908), and Hoplias, were captured
rupts the natural drift of eggs and larvae to the downstream regions
in nearly all sampling periods, suggesting that the reproductive
where growth takes place, reducing the reproductive success of fish
species and preventing gene flow. Even small dams can affect migra-
reproductive periods (Suzuki, Vazzoler, Marques, Lizama, & Inada,
tory fish reproduction, especially in periods with minimal floods,
2004) and are less dependent on specific conditions. Teles and
because they become impassable without a river level rise and hamper
Godinho (1997) reported that S. brandtii is able to breed throughout
the flood pulse, which, no matter how small, is important for spawning
the year in the Três Marias reservoir, similar to Hoplias malabaricus
and recruitment. Therefore, the establishment of priority areas for the
(Bloch 1794; Azevedo & Gomes, 1942).
conservation of migratory species in the region should consider
The results of this study indicate that the density of eggs and
spawning, reproductive seasonality, and mapping the areas where fish
larvae were correlated to increased flow and rainfall in places with
larvae grow, as well as exploring, for each site, the importance of var-
the highest record of reproductive activity of migratory species (PA1
ious environmental variables that directly or indirectly interfere with
and PIC), and in the stretch where the larvae drift from these tribu-
the reproductive process, thus ensuring the environmental integrity
taries (PA5). These environmental variables were the main causes for
considering the various disturbances.
the significant correlations found along the PCA axes. This suggests
that in atypical low flow periods, the river flow possibly increases,
although with less intensity, as a sudden short duration pulse, similarly
The authors wish to thank Companhia Energética de Minas Gerais
to the occurrence during December of this study. This sudden increase
(CEMIG) (project P&D GT 455) and Fundação de Amparo à Pesquisa
in flow rate can promote the final gonadal maturation and trigger
de Minas Gerais (FAPEMIG) (project APQ 02468‐10) for funding this
immediate spawning, as opposed to longer periods of flooding that
project and Coordenação de Aperfeiçoamento de Pessoal de Ensino
can promote breeding over a longer period (Bailly et al., 2008). Envi-
Superior (CAPES) for the grant given to the first and second authors.
ronmental variables, such as temperature and photoperiod, are also
The authors also wish to thank the Dr. Angelo Agostinho and Dr. Paulo
notorious for their relationship to the development and maturation
Pompeu for the considerations they gave in this work.
of the gonads, acting as triggers for spawning (Castro et al., 2002;
Nascimento & Nakatani, 2006; Suzuki et al., 2004; Vazzoler &
Menezes, 1992). However, in response to the low variation in water
level, the temperature and other environmental parameters showed
little variation and did not provide striking biological responses in the
egg and larvae densities. Silva et al. (2014) found no detectable effects
on ichthyoplankton density in relation to water temperature and
discharge due to insufficient variation of these environmental
parameters. The fact that this study was carried out during only one
seasonal period (the rainy season) also explains the lack of variability
and the consequent absence of a clear relationship to spawning, as
described by Suzuki and Pompeu (2016). However, through PCA, a
distinction between the environmental parameters of the tributaries
and the main river was observed, except for the upper Pará River
section (PA1), which could explain the preference for spawning in the
tributaries such as the Picão River (PIC) with high TDS and conductivity
values. In the upstream areas of the larger rivers, migratory species
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How to cite this article: Rosa GR, Salvador GN, Bialetzki A,
ichthyoplankton during an unusual period of low flow in a tributary of the São Francisco River, Brazil. River Res Applic. 2017.
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