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Acta Scientiarum 

 

http://www.uem.br/acta 
ISSN printed: 1679-9283 
ISSN on-line: 1807-863X 
Doi: 10.4025/actascibiolsci.v39i3.33021 

 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 339-347, July-Sept., 2017 

Ovarian histology and fecundity in the evaluation of the 

reproduction of the invasive species Serrasalmus marginatus 

(Characidae) on a neotropical floodplain  

Gabriele Sauthier Romano de Melo

1

, Herick Soares de Santana

2

 and Claudenice Dei Tos

3*

 

1

Curso de graduação em Ciências Biológicas, Departamento de Biologia, Universidade Estadual de Maringá, Maringá, Paraná, Brazil. 

2

Programa 

de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Universidade Estadual de Maringá, Maringá, Paraná, Brazil. 

3

Departamento de Biologia, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá, Av. Colombo, 5790, 

87020-900, Maringá, Paraná, Brazil. *Author for correspondence. E-mail: claudenice@nupelia.uem.br 

ABSTRACT. The construction of the Itaipu Hydroelectric Power Plant in 1982 led to the formation of a 
reservoir, which, in turn, leveled the waters of the Paraná River by flooding the geographic barrier Salto de 
Sete Quedas. This allowed the piranha Serrasalmus marginatus to invade and colonize the upper Paraná 
River. This study aimed to: i) confirm, through light microscopy, the reproductive phases of S. marginatus 
females; ii) estimate fecundity and iii) evaluate the reproduction areas of the population. A total of 764 
females were collected from nine sampling sites on the upper Paraná River floodplain. Microscopic analysis 
of the ovaries showed the following phases: early developing subphase, developing phase, spawning capable 
phase, actively spawning subphase, regressing phase and regenerating phase. The frequency distribution of 
the oocytes shows that spawning is fractional and fecundity indeterminate. Fecundity varied from 410 to 
752 oocytes (mean = 584). The continual spawning of oocytes during the long reproductive period, as well 
as the aggressiveness of the species as regards the defense of its offspring, guarantees more descendants in 
the Patos, Ventura, Fechada, Guaraná and Garças lagoons and Ivinheima and Baia rivers of the upper 
Paraná River floodplain.

 

Keywords: Indeterminate fecundity, type of spawning, oogenesis, oocytes, piranha. 

Histologia ovariana e fecundidade na avaliação da reprodução da espécie invasora 
Serrasalmus marginatus (Characidae) em uma planície de inundação neotropical 

RESUMO. A construção da Usina Hidroelétrica de Itaipu, em 1982, levou a formação do reservatório que 
por sua vez nivelou as águas do rio Paraná inundando a barreira geográfica do salto de Sete Quedas. Isto 
permitiu que a piranha Serrasalmus marginatus invadisse e colonizasse o alto rio Paraná. Este estudo teve por 
objetivos: i) confirmar através da microscopia de luz as fases reprodutivas das fêmeas de S. marginatus; ii) 
estimar a fecundidade e iii) avaliar as áreas de reprodução da população. Um total de 764 fêmeas foram 
amostrados em nove estações de amostragem na planície de inundação do alto rio Paraná. A análise 
microscópica dos ovários mostrou fêmeas nas subfases em desenvolvimento inicial, fase desenvolvimento, 
fase apto à desova, subfase desova ativa, fase regressão e fase regeneração. A distribuição de frequência dos 
oócitos mostra que a desova é parcelada e a fecundidade é indeterminada. A fecundidade variou de 410 a 
752 e em média 584 oócitos. A desova contínua durante o longo período reprodutivo associado à 
agressividade em relação à defesa da prole garante o sucesso em deixar mais descendentes nas lagoas dos 
Patos, Ventura, Fechada, do Guaraná, das Garças, nos rios Ivinheima e Baia da planície de inundação do alto 
rio Paraná. 

Palavras-chave: Fecundidade indeterminada, tipo de desova, oogênese, oócitos, piranha. 

Introduction 

Invasion of species is one of the main causes of 

biodiversity loss leading to both environmental and 
economic damage (McNeely, 2001; Molnar, 
Gamboa, Revenga, & Spalding, 2008; Pejchar & 
Mooney, 2009; Keller, Geist, Jeschke, & Kühn, 
2011; Simberloff et al.,  2013).  Invasive species have 

some characteristics that facilitate or allow their 

establishment in a new environment (e.g. high 

trophic plasticity and dispersion capacity) (Lodge, 

1993; Marchetti, Moyle, & Levine, 2004). As regards 

freshwater ecosystems, fish have received special 

attention due to the quantity of invasive species 

recorded in recent years, especially carp, tilapia and 

African    catfish    (Garcia,    Loebmann,   Vieira,   & 

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340 

Melo et al. 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 339-347, July-Sept., 2017 

Bemvenuti, 2004; Vitule, Umbria, & Aranha, 2006; 
Russel, Thuesen, & Thomson, 2012). 

The upper Paraná River, possessing high species 

richness, according to Langeani et al. (2007), 
underwent a massive invasion due to the formation 
of the Itaipu Reservoir, which eliminated the natural 
geographic barrier Salto de Sete Quedas (Júlio Jr, 
Dei Tos, Agostinho, & Pavanelli, 2009), which had 
separated the faunas of the middle and upper Paraná 
River. Consequently, about 33 species became 
invaders, characterizing one of the largest invasions 
of freshwater species in South America (Skóra, 
Abilhoa, Padial, & Vitule, 2015).  

With the flooding, the piranha Serrasalmus 

marginatus Valenciennes, 1837 successfully colonized 
the upper Paraná River basin. Its success increased 
with the construction of the Piracema Channel in 
the Itaipu Reservoir, where this species has been 
recorded (Makrakis, Gomes, & Makrakis, 2007). It is 
distributed in the Paraná-Paraguay river basin, lives 
in both lentic and lotic environments, carries out 
short-distance migrations (Graça & Pavanelli, 2007) 
and has been indicated as the principal cause of the 
decrease in the population of its native congener 
(Agostinho & Júlio Jr, 2002). In addition, S. 
marginatus
 is an iteroparous, gonochoristic, 
monomorphic, oviparous species with external 
fecundation. It reaches sexual maturity at 11.5 cm 
standard length for males and 12.2 cm standard 
length for females and all individuals are able to 
reproduce at 13.0 cm standard length (Suzuki, 
Vazzoler, Marques, Lizama, & Inada, 2004). 
Moreover, it possesses batch spawning, parental care 
and a long reproductive period (September to April) 
(Vazzoler, 1996; Suzuki et al., 2004), coinciding with 
the season of higher temperatures and flooding. 

One way to evaluate the reasons for the success 

of  S. marginatus is to study its reproductive activity 
and capacity, since reproducing and maintaining the 
population is one of the precepts for obtaining 
success in a new environment. The reproductive 
capacity of fish can be quantified using the following 
measurements: maturation length or age, type of 
fecundity, fecundity, duration of the reproductive 
season, spawning behavior, and spawning fraction. 
Information about reproductive potential is 
fundamental to spawning stock biomass evaluation 
(Hunter, Macewicz, Lo, & Kimbrell, 1992; Murua et 
al., 2003; Ganias, 2013; Ganias, Lowerre-Barbieri, & 
Cooper, 2015). Thus, this work aims to: i) validate 
the reproductive phases of the females using light 

microscopy; ii) estimate the fecundity and iii) 
evaluate the reproduction areas of the S. marginatus 
population from the upper Paraná River floodplain. 

Material and methods 

Study area 

The upper Paraná River floodplain is located 

downstream from the Engenheiro Sérgio Mota 
(Porto Primavera) Hydroelectric Power Plant and 
upstream from the Itaipu Reservoir. This distance 
(approximately 250 km) is the last dam-free stretch 
of the Paraná River in Brazil (Agostinho & Zalewski, 
1996). Although the floodplain is located between 
two large dams, the Paraná River possesses two 
important tributaries, the Baia and Ivinheima rivers, 
which contribute to the maintenance of biodiversity 
and ideal conditions for the entire aquatic fauna, 
mainly the ichthyofauna.  

Sampling 

The fish were collected quarterly (March, June, 

September and November/December 2013, 2014 

and 2015) from 9 sampling sites on the upper Paraná 

River floodplain: 1 - Baia River (Rbai), 2 - 

Ivinheima River (Rivi), 3 - Paraná River (Rpar), 4 - 

Guaraná Lagoon (Lgua), 5 - Patos Lagoon (Lpat), 6 - 

Paraná River in the Garças Lagoon (Lgar), 7 - 

Ressaco do Pau Veio Lagoon (Lpve), 8 - Baia River 

in the Fechada Lagoon (Lfec) and 9 - Ivinheima 

River in the Ventura Lagoon (Lven) (Figure 1).  

The samplings were carried out using 11 gill nets 

(meshes: 2.4; 3; 4; 5; 6; 7; 8; 10; 12; 14; 16 cm, 

between opposite knots) and two trammel nets 

(meshes: 6; 8 cm). The nets were exposed for 24 

hours at every site and checked between 8:00 and 

9:00 (night-morning), 16:00 and 17:30 (daytime) 

and 22:00 and 23:30 (evening-night). In addition, 

bottom otter trawls (20 m long; 0.5 cm mesh) were 

carried out during the day in the coastal areas of 

every lagoon. The fish were anesthetized and 

euthanized using 0.1% ethyl aminobenzoate 
(benzocaine), according to the protocols of 

Summerfelt and Smith (1990) and approved by 

CEUA (Committee for the Ethical Use of Animals) 

(Universidade Estadual de Maringá). 

The following data were recorded for each 

individual: catch site, catch date, standard length 
(cm), total weight to the nearest 0.01 g, gonadal 
development phases based on the macroscopic 
characteristics of the ovary, total weight of the 
gonads (twg) to the nearest 0.01 g and weight of the 
ovarian fractions (wof) to the nearest 0.01 g. 

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Figure 1. Study area and location of the sampling sites (Baia River – 1; Ivinheima River – 2; Paraná River – 3; Guaraná Lagoon – 4; Patos 
Lagoon – 5; Garças Lagoon – 6; Ressaco do Pau Veio Lagoon – 7; Fechada Lagoon – 8; Ventura Lagoon – 9) on the upper Paraná River 
floodplain. 

Reproductive characterization 

The ovarian development phases were attributed 

according to the macroscopic characteristics 

proposed by Brown-Peterson, Wyanski, Saborido-

Rey, Macewicz, and Lowerre-Barbieri (2011), 

Wildner, Grier, and Quagio-Grassiotto (2013) and 

Quagio-Grassiotto, Wildner, and Ishiba (2013). A 

fraction of the left lobe of the ovary was fixed in 

Bouin solution for at least 48 hours, dehydrated in 

ethanol, infiltrated using Historesin and shaped into 

blocks, which were cross-sectioned at a thickness of 

5  μm and stained using 0.5% Toluidine Blue, 

Hematoxilin/Eosin and periodic acid Schiff/ 

hematoxylin/metanil yellow (Quintero-Hunter, 

Grier, & Muscato, 1991). The germ cells were 

identified according to Grier, Uribe-Aranzábal, and 

Patiño (2009) and Wildner et al. (2013) and the 

reproductive phases attributed macroscopically 
(early developing subphase, developing phase, 

spawning capable phase, actively spawning subphase, 

regressing phase and regenerating phase) were 

validated by the microscopic characteristics of the 

development stages of more advanced cell types, 

according to Brown-Peterson et al. (2011), Quagio-

Grassiotto et al. (2013) and Wildner et al. (2013).  

In order to determine type of fecundity, ovaries 

from individuals in the developing phase, spawning 
capable phase and actively spawning subphase were 
selected. The right lobe of the ovary was fixed in 
10% buffered formalin. Using the gravimetric 
method, the oocytes were counted and measured 
from three subsamples of approximately 0.3 g each 
from the anterior, middle and posterior region of 
the right lobe of the ovary (Hunter, Lo, & Leong, 
1985; Murua et al., 2003). 

The diameter of the oocytes from 12 specimens 

of  S. marginatus was measured using a 
stereomicroscope equipped with an ocular 
micrometer to determine the type of oocyte 
development and spawning. The type of spawning 
was determined according to the frequency 
distribution of the oocytes per diameter class 
(Murua & Saborido-Rey, 2003). 

Thus, absolute fecundity (AF), i.e. the number 

of oocytes that a female will spawn in the next 
reproductive period, was calculated according to 
Vazzoler (1996). 

The floodplain reproduction sites were identified 

by number of females in different reproductive 
phases. 

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Results 

A total of 765 females with 3.9 to 24.9 cm 

standard length were used for macroscopic 

characterization of the gonads at the different sites of 

the floodplain. The sites having the greatest 

representativeness were Patos Lagoon (231 

individuals), Ivinheima River (214) and Ventura 

Lagoon (70). In the Baia River, 145 individuals were 

collected, while 51 and 18 were collected in the 

Fechada and Guarana lagoons, respectively. The 

sites having the fewest number of samples were the 

Garças Lagoon, Paraná River, and Ressaco do Pau 

Veio Lagoon, with eight, twenty-three and five 

individuals, respectively.  

Based on the microscopic diagnosis of the germ 

lineage, cysts with a batch of oogonia surrounded by 

prefollicle cells, pachytene oocytes, primary growth 
oocytes, early and late secondary growth oocytes, a 
full-grown oocyte (Figure 2 and Table 1) and oocyte 
maturation (Figure 3J) were recognized in S. 
marginatus
. The postovulatory follicle complex 
recorded after ovulation and follicular atresia 
showed oocytes unable to ovulate (Figure 2H, I). 

Histological sections of the ovaries showing the 

development phases were detailed and described 
(Figure 3 and Table 2). 

The diameter of the vitellogenic oocytes of S. 

marginatus varied from 300 to 1700 μm (Figure 4), 
and the trends reveal asynchronous development of 
the oocytes and batch spawning. Only a portion of 
the oocytes is spawned in each batch after reaching 
maturation and ovulation. 

 

 

Figure 2. Oocyte development in Serrasalmus marginatus. Light microscopy, PAS/Hematoxylin/ Metanil Yellow (A, B, F, G, H, I), 

Hematoxilin/Eosin (C, E) and Toluidine Blue (D). (A) Nest of oogonia is surrounded and among pre-follicle cells, forming germline 
cysts. Inside this nest the oogonia are spherical and voluminous and their nucleus widens with an evident nucleolus, bar = 22 μm. (B) 
Cell nest with pachytene oocytes, bar = 29 μm. (C) Ovarian follicle with primary growth oocyte, bar = 70 μm. (D) Late primary growth 
oocyte shows the beginning of the formation of the cortical alveoli, bar = 145 μm. (E) Early secondary growth oocyte begins the 
deposition of yolk, formation of the cortical alveolus, bar = 295 μm. (F), Late secondary growth oocyte, bar = 295 μm. (G) Full-grown 
oocyte, bar = 590 μm. (H) The postovulatory follicle complex, bar = 295 μm. (I) Follicular atresia, bar = 295 μm.  CA, cortical alveoli; 
AF, atretic follicle; BM, basement membrane; F, follicle cell; FG, full-grown oocyte; LO, leptotene oocytes; N, nucleus; NU, perinuclear 
nucleoli; OF, ovarian follicle; OG, oogonium; OL, ovarian lumen; PF, prefollicle cells; PG, primary growth oocyte; PO, pachytene 
oocyte; SG, secondary growth oocyte; Y, yolk globule; ZP, zona pellucida. 

 

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Figure 3. Reproductive phases of the ovarian cycle of Serrasalmus marginatus according to oocyte differentiation stages. Light Microscopy, 
Toluidine Blue (A, B, C, G, H, I, M, N, O) and PAS/Hematoxylin/Metanil Yellow (D, E, F, J, K, L, P, Q, R). (A) Early development 
subphase, stroma contains primary and secondary oocytes, bar = 550 μm. (B) Lamella contains early secondary growth oocytes, bar = 140 
μm. (C) Oogonia nest in the germinal epithelium, bar = 70 μm. (D) Developing phase, primary and secondary growth oocytes, bar = 600 
μm. (E) Secondary growth oocytes present cortical alveoli and yolk globules, bar = 300 μm. (F) Oocytes with numerous cortical alveoli, 
bar = 150 μm. (G) Spawning capable phase, shows primary growth and full-grown oocytes, bar = 550 μm. (H) Full-grown oocyte with 
central nucleus, bar = 280 μm. (I) Full-grown oocyte showing amicropyle, bar = 140 μm. (J) Actively spawning subphase, showing a 
mature oocyte, bar = 600 μm. (K) Postovulatory follicle complex and primary growth oocytes, bar = 300 μm. (L) Postovulatory follicle 
complex, bar = 80 μm. (M) Regressing phase, bar = 550 μm. (N) Atretic follicle, bar = 280 μm. (O) Atretic follicle and primary growth 
oocyte, bar = 140 μm. (P) Regenerating phase, bar = 600 μm. (Q) Primary growth oocyte, bar = 270 μm. (R) Postovulatory follicle 
complex, primary growth oocyte and oogonia nest, bar = 6 μm. AF = atretic follicle; CA = cortical alveolus; F = follicle cells; FG = full-
grown oocytes; Mi = micropyle; MO = maturing oocyte; N= nucleus/germinal vesicle; NC = nest of oogonia; Nu = nucleolus; OG = 
oogonium; OL = ovarian lumen; OW = ovarian wall; PG = primary growth oocytes; POC = postovulatory follicle complex; SG = 
secondary growth oocytes; Y = yolk globules; ZP = zona pellucida. 

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Table 1. Diagnosis of germinal cells in different stages of oocyte 
development, postovulatory follicle complex (POC) and atretic 
ovarian follicles of Serrasalmus marginatus on the Paraná River 
floodplain. 

Stages/POC/Atresia Microscopic 

Characteristics 

Primary growth 

Ovarian follicle with primary  growth oocyte. It

shows intense basophilic ooplasm and the nucleus or

germinal vesicle with several perinuclear nucleoli 

(Figure 2C). A gradual increase of ooplasm and the

appearance of cortical alveoli record the end of

primary growth oocytes (Figure 2D). 

Early secondary 

growth 

This oocyte (Figure 2E) is showing the gradual

increase of yolk in the ooplasm and cortical alveoli 

are arranged on the periphery of the ooplasm during

development. 

Late secondary 

growth 

Late secondary  growth oocyte has nuclear outline

more irregular, cortical alveoli are seen on periphery

of ooplasm and zona pellucida more developed

(Figure 2F). 

Full-grown oocyte  This oocyte (Figure 2G) contains a slightly eccentric 

nucleus, surrounded by ooplasm completely full of

yolk globules and the cortical alveoli develop as a thin

peripheral layer in the ooplasm. 

Postovulatory follicle 

complex 

After oocyte maturation the evidence of ovulation in

the ovarian stroma was the formation of the

postovulatory follicle complex observed in the

lamella (Figure 2H). 

Follicular atresia 

Unovulated  oocyte becomes atretic and its

degeneration and removal from the ovarian follicle

occurs (Figures 2I). 

 

Table 2. Phases and subphases of reproduction based on the 
microscopic characteristic of germinal cells of Serrasalmus 
marginatus
 females on the Paraná River floodplain. 

Phase/subphase Microscopic 

Characteristics 

Initial 

Development 

subphase 

Ovarian stroma contains more primary growth oocytes 

(PG) and some secondary growth oocytes (SG) (Figure 

3A). In the SG the cortical alveoli and formation of yolk 

globules begins to appear (Figure 3B). Nests containing 

oogonia in proliferation are observed at the edge of 

ovarian lumen (Figure 3C). 

Developing 

Primary and secondary growth oocytes (Figure 3D). In 

the early and late vitellogenic oocytes, the formation 

of yolk globules progressed in their oolema (Figure 

3E, F). 

Spawning Capable Primary growth and secondary growth (early, late 

vitellogenic and full-grown oocytes) (Figure 3G). Full-

grown oocytes with nucleus situated at the center of the 

ooplasm. Its yolk globules abundant except on 

periphery (Figure 3H). Micropyle recorded in the full-

grown oocytes (Figure3I). 

Actively Spawning 

subphase 

Maturing oocyte with germinal vesicle takes an 

eccentric position on the periphery of the ooplasm at 

the animal pole near the micropyle (Figure 3J). In this 

subphase atretic follicle and postovulatory follicle 

complex also occur (Figure 3K, L). 

Regression 

Predominance of primary growth oocytes and atretic 

follicles (Figure 3M, N, O), and an absence of 

secondary growth oocytes. 

Regeneration 

Presence of primary growth oocytes, proliferating 

oogonia forming cell nests and degenerating 

postovulatory follicles were recorded (Figure 3P, Q, R).

 

The diameter of the vitellogenic oocytes of S. 

marginatus varied from 300 to 1700 μm (Figure 4), 
and the trends reveal asynchronous development of 
the oocytes and batch spawning. Only a portion of 
the oocytes is spawned in each batch after reaching 
maturation and ovulation. 

 

Figure 4. Frequency of the vitellogenic oocyte diameter (μm) of 

the ovaries of the piranha Serrasalmus marginatus sampled on the 
upper Paraná River floodplain. 

The absolute fecundity estimated for six 

individuals whose total length varied from 16.4 to 

20.2 cm, varied from 410 to 752 oocytes. As regards 

the different rivers of the upper Paraná River 

floodplain, the piranha S. marginatus shows 

reproductive activity in every studied environment; 

however, it is more frequent in Patos Lagoon and 

the Ivinheima and Baia rivers, successfully 

occupying the lotic waters of the rivers and the 

lentic waters of the lagoon (Figure 5). Among the 

principal environments (Ivinheima, Baia and 

Paraná), S. marginatus is least reproductively active in 

the Paraná River. The main channel of the Paraná 

River did not have any individuals in advanced 

stages of gonadal development (Figure 5). 

 

 

Figure 5. Spatial distribution of the gonadal development phases 

per river and sampling site of the piranha Serrasalmus marginatus 
sampled on the upper Paraná River floodplain. Lpat = Patos 
Lagoon; Lven = Ventura Lagoon; Rivi = Ivinheima River; Lfec 
= Fechada Lagoon; Lgua = Guaraná Lagoon; Rbai = Baia River; 
Lgar = Garças Lagoon; Lpve = Pau Veio Lagoon; Rpar = Paraná 
River.

 

Discussion 

A fish must allocate time and resources for 

reproduction to be represented genetically in the 

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next generation (Wootton, 1998). The reproductive 
success of fish thus depends on their reproductive 

rate, the survival rate of their descendants until the 

age of reproduction, spawning type and number of 

reproductive opportunities (Wootton, 1998; Murua 

& Saborido-Rey, 2003; Lowerre-Barbieri, 2009). 

The reproductive strategy of S. marginatus may be 

considered opportunist, which is characteristic of 

species that have a short gestation period, are small 

in size and invest little in their offspring (Winemiller 

& Rose 1992; Winemiller, 2005), enabling them to 

rapidly populate different habitats and invade new 

ones. The capacity to spawn during the entire 

reproductive season is a species life-history trait that 

allows the maintenance of population levels even in 

situations of environmental disturbance (e.g. 

suppression of Sete Quedas barrier that permitted 

the passage of species from the middle to upper 

Paraná River (Júlio Jr et al., 2009)). 

Over each reproductive cycle, the renewal of 

germ cells, their differentiation, development, 
maturation and release result in gonadal alterations 
that characterize different reproductive phases. The 
reproductive phases attributed macroscopically to S. 
marginatus
 were confirmed through light 
microscopy. They are developing, spawning capable, 
regressing and regenerating, according to Brown-
Peterson et al. (2011). These phases are used 
because they are simpler and in Brazil have been 
adopted by Wildner et al. (2013) for Serrasalmus 
maculatus
, Quagio-Grassiotto et al. (2013) for Hoplias 
malabaricus
 and Sorubim lima and Agostinho et al. 
(2015) for Hemiodus orthonops.  

Fish species with asynchronous ovarian 

development exhibit strategies of determinate or 
indeterminate fecundity (Hunter et al., 1985; Murua 
et al., 2003; Murua & Saborido-Rey, 2003). These 
strategies relate to the pattern and time lag in which 
the pre-vitellogenic oocytes (primary growth) are 
recruited to compose the stock of vitellogenic 
oocytes (secondary growth). In indeterminate 
fecundity, vitellogenesis continues after the start of 
spawning (Hunter et al., 1985; Murua & Saborido-
Rey, 2003; Murua et al., 2003; Ganias et al., 2015).  

The fecundity of the batches, spawning 

frequency and duration of the reproductive season 
must be known to estimate indeterminate fecundity 
(Hunter et al., 1992; Murua & Saborido-Rey, 2003; 
Murua et al., 2003). The patterns of total spawning 
and partial spawning and the type of fecundity 
(determinate or indeterminate) have been recorded 
for marine and freshwater species (Brown-Peterson 
et al., 2011). Among the 41 species from the upper 
Paraná River that were studied as regards spawning 

type, 73% possess batch spawning and, therefore, 
indeterminate fecundity (Vazzoler, 1996).  

The frequency of the diameter of the oocytes 

and the microscopic record of the different types of 
oocytes that develop in the reproductive cycle show 
that their development is asynchronous in S. 
marginatus
; therefore, it exhibits a reproductive 
strategy of batch spawning and indeterminate 
fecundity. Fecundity (estimated) varying from 410 to 
752 has guaranteed the reproductive success of this 
species. This strategy of batch spawning and 
indeterminate fecundity has been recorded for 
Loricariichthys castaneus (Gomes, Araújo, Uehara, & Sales, 
2011) and Serrasalmus maculatus (Wildner et al., 2013). 

Adequate environmental conditions and sites for 

larval development and juvenile growth are 
fundamental to the population success of any 
species. Our results demonstrate that most of the 
reproductive stages predominate in the Baia and 
Ivinheima rivers, mainly spawning capable 
individuals, which are in great number in the 
lagoons associated with these two rivers. These 
rivers belong to the upper Paraná River floodplain 
and are two of the main tributaries responsible for 
the maintenance of ichthyofaunistic diversity and 
serve as nursery and growth areas, mainly for 
migratory species (Agostinho, Thomaz, Minte-Vera, 
& Winemiller, 2000; Reynalte-Tataje, Agostinho, & 
Bialetzki, 2013). Therefore, these sites are 
characterized by possessing adequate conditions for 
the establishment of S. marginatus and, consequently, 
the population increase of this species results in 
negative impacts for the native species S. maculatus
as the two are congeners that have similar 
environmental and feeding requirements (Agostinho 
& Júlio Jr, 2002; Agostinho, 2003; Alexandre, Luiz, 
Piana, Gomes, & Agostinho, 2004).  

Conclusion 

The reproductive success of S. marginatus on the 

upper Paraná River floodplain is attributed to 
parental care and greater aggressiveness in defending 
its feeding and reproduction territories (Agostinho, 
2003; Alexandre et al., 2004). However, it is also 
associated with fecundity, because the long 
reproductive period with the continual spawning of 
oocytes guarantees more descendants. Serrasalmus 
marginatus
 reproduction is intense in lotic (river) 
environments and moderate in channels and lagoons 
of the upper Paraná River floodplain (Vazzoler, 
1996; Agostinho, 2003; Suzuki et al., 2004). This 
study reveals that its reproductive success continues 
to be recorded in the Ivinheima River and in the 
lagoons of the upper Paraná River floodplain. 

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346 

Melo et al. 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 339-347, July-Sept., 2017 

Acknowledgements 

We thank Dr. Liliana Rodrigues for the support 

received by the Programa de Pesquisa Ecológica de Longa 

Duração (PELD) and the Núcleo de Pesquisas em 

Limnologia, Ictiologia e Aquicultura (Nupélia) for 

technical personnel, researchers and logistical 

support. Dr. Luiz C. Gomes provided financial 

support. We also thank the Fundação Araucária for 

granting a scientific initiation scholarship to 

Gabriele S. R. de Melo, the Complexo de Centrais de 

Apoio à Pesquisa (COMCAP) for equipment support 

and the anonymous reviewers for their helpful 

comments. 

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Received on August 8, 2016. 
Accepted on March 9, 2017. 

 

 

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