Scientific Article
ISSN 1678-2305 online version
BOLETIM DO INSTITUTO DE PESCA
Ávila-Simas et al. Bol. Inst. Pesca 2019, 45(2): e484. DOI: 10.20950/1678-2305.2019.45.2.484 1/12
FISH PREDATORS OF THE GOLDEN MUSSEL Limnoperna fortunei
IN DIFFERENT ENVIRONMENTS IN A SOUTH AMERICAN
SUBTROPICAL RIVER
ABSTRACT
This study aimed to evaluate whether the golden mussel, Limnoperna fortunei, identified in the upper
Uruguay River for the first time in 2012, has been incorporated into the diet of the ichthyofauna
present in different environments of a Neotropical reservoir. To achieve this, we analyzed the
digestive tract of fish that were collected seasonally between August 2015 and May 2016. The results
showed that 22 fish species had L. fortunei in the digestive tract, of which 11 were previously not
known to comprise the diet of this mollusk. Furthermore, it was observed that species belonging
to the orders Characiformes and Cichliformes were the main consumers of L. fortunei in the lentic
environment, whereas in the lotic and transition environments, the main consumers belonged to
the order Siluriformes. The degree of digestion of L. fortunei in the digestive tract of fish indicated
that although most fish could digest this food resource, some Siluriformes found it difficult. Thus,
it can be concluded that the availability of L. fortunei in the upper Uruguay River forms a new food
resource for the endemic ichthyofauna.
Key words: biological control; fish feeding; invasive species; neotropical fishes; potential predators;
Uruguay River.
PEIXES PREDADORES DO MEXILHÃO-DOURADO Limnoperna fortunei EM
DIFERENTES AMBIENTES DE UM RIO SUBTROPICAL DA AMÉRICA DO SUL.
RESUMO
O presente estudo teve como objetivo avaliar se o mexilhão-dourado Limnoperna fortunei,
identificado na região do alto rio Uruguai pela primeira vez em 2012, vem sendo incorporado
na dieta da ictiofauna presente nos diferentes compartimentos de um reservatório neotropical.
Para isto, foi analisado o trato digestório de peixes através de coletas sazonais realizadas entre
agosto de 2015 e maio de 2016. Os resultados mostraram que 22 espécies de peixes apresentaram
L. fortunei no trato digestório, sendo que o registro de consumo deste molusco era desconhecido
para 11 delas. Além disso, foi possível observar que espécies das ordens Characiformes e
Cichliformes foram as principais consumidoras de L. fortunei no ambiente lêntico, enquanto
que nos ambientes lóticos e de transição (lótico/lêntico) os principais consumidores deste
mesmo recurso foram espécies pertencentes a ordem Siluriformes. Quando avaliado o grau de
digestão de L. fortunei encontrado no trato digestório dos peixes, foi observado que a maioria
dos peixes consegue digerir esse recurso alimentar, entretanto, merece destaque o fato de que
algumas espécies de Siluriformes encontram dificuldade em digerir esse molusco invasor. Diante
dessas informações é possível concluir que a disponibilidade de L. fortunei no alto rio Uruguai
vem proporcionando uma nova oferta de alimento para diferentes espécies de peixes, e que os
consumidores variam de acordo com o compartimento do reservatório.
Palavras-chave: alimentação de peixes; controle biológico; espécies invasoras; peixes neotropicais;
potenciais predadores; rio Uruguai.
INTRODUCTION
The South American freshwater ichthyofauna are characterized by high feeding
plasticity, using a wide variety of food resources present in aquatic (including many
species of vertebrates, invertebrates, microorganisms, and primary producers) as well
as terrestrial (including leaves, fruits, seeds, and insects) environments (Petry et al.,
Sunshine de Ávila-Simas
1
David Augusto Reynalte-Tataje
2
Evoy Zaniboni-Filho
1
1
Universidade Federal de Santa Catarina – UFSC,
Laboratório de Biologia e Cultivo de Peixes de
Água Doce – LAPAD, Rodovia Francisco Thomaz
Dos Santos, 3532, Armação do Pântano Do
Sul, CEP 88066-260, Florianópolis, SC, Brasil.
E-mail: sunshine_avila@hotmail.com (corresponding
author).
2
Universidade Federal Fronteira Sul – UFFS, Centro de
Ciências Biológicas, Av. Jacob Reinaldo Haupenthal,
1580, São Fernando, CEP 97900-000, Cerro Largo,
RS, Brasil.
Recebido: Setembro 20, 2018
Aprovado: Março 11, 2019
FISH PREDATORS OF THE GOLDEN MUSSEL...
Ávila-Simas et al. Bol. Inst. Pesca 2019, 45(2): e484. DOI: 10.20950/1678-2305.2019.45.2.484 2/12
2011). In addition, trophic opportunism is also a key attribute
among these fish, which may benefit from certain unusual food
resources in their diet that are widely available in the environment
either temporarily or permanently (Oliveira et al., 2010).
A few years ago, the golden mussel Limnoperna fortunei
(Dunker, 1856), a bivalve from Southeast Asia, was recorded in
South America (Pastorino et al., 1993). In the following years,
its presence was reported in the Itaipu hydroelectric power plant
(Darrigran and Mansur, 2009) and in reservoirs in the state of
São Paulo (Avelar et al., 2004). More recently L. fortunei was
also found in the São Francisco river basin (Barbosa et al., 2016).
Currently, L. fortunei is considered the freshwater bivalve
responsible for the greatest economic and environmental impacts
in South America, similar to Dreissena polymorpha (zebra mussel)
in North America (Darrigran and Damborenea, 2005).
The high reproductive capacity and absence of natural predators
of L. fortunei have aided the development of large population
clusters of this organism (Darrigran, 2002), which can result in
changes in the trophic chain of ecosystems where this species is
established (Brugnoli et al., 2005). Fish species with morphological
characteristics for a malacophagous diet, or that have the capacity
to break the shells of these molluscs tend to have a greater success
in the consumption of this food resource (Oliveira et al., 2010).
Previous studies conducted at different sites detected changes in
the diet of fish that consumed the golden mussel (Cantanhêde et al.,
2008; Oliveira et al., 2010; Lopes and Vieira, 2012). These changes
could be motivated only by the presence of the golden mussel or
also by the reduction in the local biodiversity, but it demonstrates
the ability of some fish species to explore this new source of food.
The presence of the golden mussel was documented by Agudo‑Padrón
(2012) in the upper Uruguay River. This region has a fish assembly
composed of more than 100 species (Zaniboni‑Filho et al., 2004).
However, there is no record that the introduction of this mollusk
caused changes in the diet of these fish.
Considering that L. fortunei is found in high densities and can
offer an abundant supply of food for fishes, especially those with
broad feeding plasticity, this study aimed to (1) assess whether
the golden mussel is consumed by the ichthyofauna in the upper
Uruguay River, by evaluating the presence of this mollusk in the
digestive tract of fish; (2) evaluate the consumption rates of golden
mussel for each fish species; and (3) analyze whether there is a
difference in L. fortunei predation by fish in environments with
different hydrological characteristics.
MATERIAL AND METHODS
Study area
Eight sampling sites were located on a stretch of approximately
350 km of the upper Uruguay, located between the municipalities
of Piratuba (SC) and Mondaí (SC). Seven of these were located
in the area of influence of the Itá Reservoir. Of these, two
were located in a lotic environment, upstream of the reservoir
(LO1 and LO2); four were inside the reservoir, of which two were
in the transition area (semi‑lentic) between the lotic and lentic
environment (TR1 and TR2) and two in the lentic environment
of the reservoir (LE1 and LE2); and one site was located on a
lotic stretch, immediately below the Itá Dam (LO3). The eighth
sampling site was located on a lotic stretch of the Uruguay River
at a distance of 206 km downstream from the Itá Dam and without
the direct influence of hydroelectric effects (LO4) (Figure 1).
Fish collection and laboratory analysis
Samples were collected between August 2015 and May 2016,
resulting in four samples at each of the eight sampled sites (totaling
32 samples). Diverse sampling equipment was used, such as gillnets
with meshes of 1.5, 2.0, 2.5, and 3.0 cm between adjacent nodes,
height of 1.6 m, and length of 10, 15, 20, and 30 mm, respectively;
crossing nets i.e., gillnets with meshes of 8.0 cm between adjacent
nodes, height of 8 m, and length of 60 to 120 m; and trammel nets
with meshes of 3.0, 4.0, and 5.0 cm between adjacent nodes, height
of 1.8 m, and length of 30 and 40 m. The capture effort was constant
over time at all sampling points, allowing the comparison of the
data. All the nets were installed at dusk and collected at dawn the
next day, remaining in the environment for 12 h. All fishes caught
were fixed in 10% formalin and later analyzed in the laboratory.
Owing to the high number of fish caught, a sub‑sampling strategy
was established, wherein a maximum of 20 specimens of each
species at each of the eight sampling sites (in each season) was
selected for further analysis.
Subsequently, the fixed fish were transferred to 70% alcohol
to measure their biometry. In the laboratory, the fishes were
identified to the lowest possible taxonomic level. The fish were
then dissected and the digestive tract removed, stored individually,
and preserved in 70% alcohol. For the analysis, only adult fish
were considered, according to Vazzoler (1996), to avoid distortions
caused by ontogenetic changes in fish feeding.
Fish diet
The digestive tract of each fish was placed individually in a
Petri dish and observed under a binocular stereomicroscope for
identification and quantification of food items. The identification
of the items was done with the aid of specialized bibliography
(McCafferty, 1983; Zaniboni‑Filho et al., 2004; Santos et al., 2012)
and through consultations with experts. In order to facilitate the
interpretation of the trophic groups among the different fish species,
the food items were grouped into seven categories: crustaceans
(Cladocera, Copepoda, Decapoda, and Ostracoda), detritus/sediment
(organic material in different degrees of decomposition from the
bottom, mud, and sand), insects (Chironomidae, Coleoptera,
Diptera, Ephemeroptera, Hemiptera, Homoptera, Hymenoptera,
Isoptera, Lepidoptera, Orthoptera, Trichoptera, and insect remains
that could not be identified), golden mussel (only adult individuals
with valves were identified), other invertebrates (Acarina, Araneae,
Gastropoda, Hirudinea, Nematoda, and Oligochaeta), fishes
(Characiformes, Cyprinodontiformes, Cichliformes, Siluriformes,
and fish remains that could not be identified), and plants (algae,
leaves, fruits, and seeds).
The frequency of occurrence (FO) of a food item was calculated
as the percentage of digestive tracts in which a given food