Content uploaded by Simone Cohen
Author content
All content in this area was uploaded by Simone Cohen on Nov 07, 2017
Content may be subject to copyright.
301 VOL. 47(4) 2017: 301 - 310
http://dx.doi.org/10.1590/1809-4392201701243
ACTA
AMAZONICA
Metazoan parasite communities of Leporinus
macrocephalus (Characiformes: Anostomidae) in
cultivation systems in the western Amazon, Brazil
Williane M. de O. MARTINS1*, Marcia C. N. JUSTO2, Melissa Q. CÁRDENAS2, Simone C. COHEN2
1 Instituto Federal do Acre, Estrada da Apadec nº1192, Bairro Nova Olinda, CEP: 69980-000, Cruzeiro do Sul, Acre, Brasil.
2 Instituto Oswaldo Cruz, Laboratório de Helmintos Parasitos de Peixes, Avenida Brasil nº 4365, Manguinhos, CEP: 21040-360, Rio de Janeiro, Brasil.
* Correspondig author: williane.mar tins@ifac.edu.br
ABSTRACT
In the Amazon, the growing demand for sh has been boosting the expansion of sh farms. However, the intensication of
cultivation can generate disequilibrium in the parasite-host environment, predisposing sh to parasitic infections. e objective
of this study was to evaluate the community structure of metazoan parasites in cultivation systems of piauçu, Leporinus
macrocephalus, in the state of Acre, Brazil. We examined 100 specimens from a semi-intensive cultivation system (earth tanks)
and 100 from an extensive system (dams). Overall 66.5% of the hosts were parasitized. We collected 1,240 parasite specimens,
classied in 15 metazoan taxa (10 monogenoidean, one digenean and four nematodes). e parasite prevalence was higher
by Monogenoidea in the dams, and by Nematoda in the earth tanks. e parasitic indexes were, in general, low and varied
among species. Monogeneoidea had higher values for quantitative and ecological descriptors of parasitism in the dams, while
Nematoda had higher values in the earth tanks. A single species of Digenea was found in the dams, with low prevalence. No
taxon was classied as central. In the dams, parasite abundance was correlated only with total sh length, while in the earth
tanks, it was positively correlated with total length, weight and condition factor of sh. e endoparasite and ectoparasite
infracommunities presented higher richness, dominance, diversity and evenness, respectively, in the earth tanks and in the
dams. is is the rst study of ecological descriptors of parasites of L. macrocephalus in the Amazon.
KEYWORDS: diversity, Digenea, Monogenoidea, Nematoda
Comunidade de metazoários parasitos de Leporinus macrocephalus
(Characiformes: Anostomidae) em sistemas de cultivo no oeste da
Amazônia, Brasil
RESUMO
Na Amazônia, a crescente demanda por pescado vem impulsionando a expansão da piscicultura. No entanto, a intensicação
dos cultivos pode gerar desequilíbrio no sistema parasito-hospedeiro-ambiente, predispondo os peixes a infecções parasitárias.
O objetivo deste estudo foi avaliar a estrutura das comunidades de metazoários parasitos de piauçu, Leporinus macrocephalus,
em sistemas de cultivo no estado do Acre, Brasil. Foram coletados 200 peixes, sendo 100 espécimes de sistema de cultivo
semi-intensivo em viveiro escavado e 100 de sistema extensivo em açude. Dos 200 hospedeiros analisados 66,5% estavam
parasitados. Foram coletados 1.240 espécimes de metazoários, classicados em quinze espécies (10 de Monogenoidea, uma
de Digenea e quatro de Nematoda). A prevalência de parasitismo por Monogenoidea foi maior em açude e por Nematoda em
viveiro. De forma geral, os índices de parasitismo foram baixos e variaram entre as espécies, com maiores valores dos descritores
quantitativos e ecológicos do parasitismo por Monogenoidea em açude e Nematoda em viveiro. A única espécie de Digenea
foi encontrada em açude e com baixa prevalência. Nenhum táxon foi classicado como central. Nos açudes, a abundância
parasitária foi correlacionada apenas com o comprimento total dos hospedeiros, e nos viveiros com o comprimento total,
peso e fator de condição dos hospedeiros. Nos viveiros, a infracomunidade de endoparasitos apresentou os maiores índices de
riqueza, dominância, diversidade e equitabilidade. Nos açudes, os ectoparasitos apresentaram os maiores índices. Este foi o
primeiro registro de índices parasitários de L. macrocephalus em sistemas de cultivo na Amazônia.
PALAVRAS-CHAVE: diversidade, Digenea, Monogenoidea, Nematoda
302 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
ACTA
AMAZONICA
INTRODUCTION
Leporinus macrocephalus Garavello and Britisk 1988
(Anostomidae), known as piauçu, is native from the Prata and
Paraguay river basins, and was introduced in sh farming in
the 1990’s in southeastern Brazil. e species has increasing
commercial prospects due to its great productive capacity
(Martins and Yoshitoshi 2003), being attractive for intensive
and semi-intensive rearing in mono and polyculture. e
species is omnivorous (Andrian et al. 1994) and adapts easily
to articial diets (Soares Júnior et al. 2013), presenting rapid
growth and good weight gain (Takahashi et al. 2004).
Fish farming in the state of Acre, in the southwestern
Brazilian Amazon, is diversied and increasing in importance
as an economic alternative, using both extensive and semi-
intensive cultivation systems. Usually, the extensive system is
used by family sh farms, with limited use of feed, low stocking
density and without water renewal. e semi-intensive system is
more costly, using articial rearing facilities with high stocking
densities, balanced diet with intensive use of feed, water renewal
and quality control, as well as other technologies.
Understanding the causal agents of parasitic diseases and
the complex relationship between environmental factors and
the hosts is important (Schalch and Moraes 2005). When
sh cultivation systems with high stocking densities have
inadequate water management, and substandard nutrition,
parasitic diseases can emerge (Schalch and Moraes 2005;
Zanolo and Yamamura 2006; Pavanelli et al. 2013; Zago et al.
2014), causing signicant losses to production. Under intense
infestations or infections, parasites can cause physiological
damage to hosts, leading to death of sh in severe cases
(Martins and Yoshitoshi 2003).
Studies on parasites of L. macrocephalus exist only for
the southeastern region of Brazil. In the state of São Paulo, a
prevalence of infection of 87.2% by Monogenoidea has been
determined in L. macrocephalus (Tavares-Dias et al. 1999).
High infection rates of L. macrocephalus by the nematode
Goezia leporini caused symptoms such as lack of appetite,
lethargy, pallidness and ascites (Martins and Yoshitoshi 2003).
A reduction of hematological characteristics was also observed
in L. macrocephalus parasitized by this species of Nematoda
(Martins et al. 2004). In natural populations of L. macrocephalus,
the presence of Rhinoxenus sp. and metacercariae of Digenea
was reported in the upper Paraná River oodplain, although no
quantitive or ecological parameters of parasitism were informed
(Takemoto et al. 2009).
ere is no information about parasites of L. macrocephalus
in cultivation systems in the Amazon. us, the objective
of the present study was to evaluate the communities and
infracommunities of metazoan parasites of L. macrocephalus in
cultivation systems in the state of Acre, in the Brazilian Amazon.
MATERIALS AND METHODS
Fingerlings of Leporinus macrocephalus were obtained
from a commercial ngerling producer in the region. ey
were reared in two sh farms in the municipality of Cruzeiro
do Sul (07°37’52’’S, 72°40’12’’W), state of Acre, Brazil,
each with a dierent cultivation system. In both cases the
sh were fed with a commercial extruded ration with 32%
gross protein, and, in the fattening phase, with an extruded
ration containing 28% gross protein. Also in both systems,
L. macrocephalus were reared in polyculture with Prochilodus
argenteus and Brycon cephalus.
In one farm the sh were reared in a semi-intensive
system. ey were distributed in three excavated rectangular
earth tanks, on rm ground, 1.20 m deep, each with an area
of 200 m2 and a volume of 240,000 liters, with water inlet
and outlet control. Water renewal occurred gradually, with a
supply of 5% of the total volume of the tanks weekly. Water
color was dingy/greenish, being dominated by grasses on the
margins. Stocking density was 1 sh/m2 of water surface. e
sh were fed twice a day.
e other farm used an extensive system. e ngerlings
were distributed into two dams which formed through
the accumulation of water from a stream. e dams were
rectangular in shape, with irregular edges, a depth of 1.50 m,
each one with an area of 300 m2, and a volume of 450,000
liters, without water inlet and outlet control. e color of the
water was dark, with grass vegetation on the margins. Stocking
density was approximately 1 sh/5m2 of water surface. In
addition to the natural food produced in the environment,
the sh received food supplementation once a day.
From June 2014 to December 2015 a cumulative sample
of 100 adult sh were collected from the earth tanks, and 100
from the dams. e collection was carried out by the local
farmers. Collection always occurred at the same time in the
morning. On each sampling occasion the dissolved oxygen
(O2D), hydrogenic potential (pH), water temperature (TºC)
and electric conductivity (EC) of the water at the collection
point were measured with multiparameter equipment (Hanna
Instruments, USA). Dierences in the water characteristics
between the two cultivation systems were analysed using
ANOVA (p<0.05).
The collected fish were kept in thermal boxes and
transported to the Fish Processing Laboratory (Laboratório
de Processamento de Pescado) at the Instituto Federal do
Acre, Cruzeiro do Sul Campus (Cruzeiro do Sul, Acre). e
sh were weighed (g), and measured for total legth (cm) and
necropsied. e gills, operculum and ns were examined for
the presence of ectoparasites, and the gastrointestinal tract for
the presence of endoparasites.
303 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
ACTA
AMAZONICA Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
For collection of Monogenoidea, the gills were removed
and placed in bowls containing water at 65 ºC and shaken;
then, alcohol was added to reach a concentration of 70%. e
parasites were collected under a stereoscopic microscope, xed
and stored in the same xative. e Digenea were cold xed
in AFA (2% glacial acetic acid, 3% formaldehyde, and 95%
of 70% alcohol), under light cover glass pressure. Nematodes
were rinsed in 0.7% NaCl solution and xed in hot AFA. e
material was taken to the Fish Helminth Parasite Laboratory
(Laboratório de Helmintos Parasitos de Peixes – LHPP) at
the Oswaldo Cruz Institute (Rio de Janeiro, Brazil) where
the helminthes were processed for light microscope studies.
Some specimens of Monogenoidea were mounted unstained in
Hoyer’s medium for study of the sclerotized parts, and others
were stained with Gomori’s trichrome and mounted in Canada
balsam. e Digenea were stained with Langeron’s alcoholic
acid carmine, dehydrated by means of ethyl alcohol series,
cleared using beechwood creosote and mounted in Canada
balsam as permanent slides. Nematodes were claried and
mounted on semi-permanent slides in phenol 50%. Specimens
were studied under a light microscope Zeiss Axioscope 2 and
the material was deposited at the Helminthological Collection
of the Oswaldo Cruz Institute (CHIOC).
To evaluate the eect of parasitism on the development
and health of the sh we determined the relative condition
factor (Kn), which is calculated from the relation between
total length (Lt) and total weight (Wt) of the sh using the
expression P = a Cb, where P = total weight, C = total length,
a = intercept and b = angular coecient (Le Cren 1951).
e coecients a and b were estimated after logarithmic
transformation of the weight and length data, and were used
for the calculation of the theoretically expected values of
weight. e condition factor was determined from the ratio
of the observed total weight (Wt) and the estimated weight
(We) as Kn=Wt/We. Dierences in condition factor between
parasitized and non parasitized sh were evaluated using
ANOVA (p<0.05).
e dispersion index (ID) was calculated in order to detect
the distribution pattern of the parasite communities in species
with a prevalence of ≥10% (Rózsa et al. 2000). e signicance
of ID for each species was tested using the d-statistic. e
dominance of each component of the communities was
determined by relative dominance (number of specimens
of a species / total number of specimens of all species in the
community) (Rohde et al. 1995).
As descriptors for the parasite community we calculated
richness of parasite species, the Brillouin diversity index (HB);
Evenness (E) in association with the diversity index, and the
Berger-Parker dominance index (d) (Magurran 2004). We also
calculated the parameters of infection as prevalence (P%), mean
intensity and parasite abundance based on Bush et al. (1997). All
descriptors were compared between cultivation systems through
the Mann-Whitney test (Zar 2010) at p < 0.05.
Parasite species were classied as central, secondary or
satellite, according to Bush and Holmes (1986). e Spearman
correlation coecient (rs) was used to determine possible
correlations of parasite abundance with length, weight and
the relative condition factor of the hosts (p < 0.05).
is study was authorized by the Brazilian Institute of
Environment and Renewable Natural Resources (IBAMA,
license nr. 396871-1/2013).
RESULTS
Overall, 133 (66.5%) of the 200 specimens of L.
macrocephalus were parasitized by at least one helminth species.
Forty-six hosts were parasitized by monogenoideans, 49 by
nematodes, and 38 by the association of monogenoideans,
nematodes and digeneans. We identied 15 helminth species,
10 belonging to Monogenoidea, one to Digenea, and four to
Nematoda, with a total of 1,040 collected specimens (Table
1), and a mean of 9.3±16.7 parasites/sh.
e prevalence of parasite infection was 73% in the earth
tanks and 19% in the dams. Nine species were common in both
systems (Table 2): Urocleidoides paradoxus Kritsky, atcher
& Boeger, 1986; Urocleidoides eremitus Kritsky, atcher &
Boeger, 1986; Jainus leporini Abdallah, Azevedo & Luque,
2012; Tereancistrum parvus Kritsky, Thatcher & Kayton,
1980; Dactylogyridae sp.1; Dactylogyridae sp.2. Procamallanus
(Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928;
Rhabdochona (Rhabdochona) acuminata (Molin 1860); and
Goezia leporini Martins & Yoshitoshi, 2003.
Two species of Monogenoidea were found only in the earth
tanks (Tereancistrum paranaensis Karling, Lopes, Takemoto
& Pavanelli, 2014 and Kritskyia eirasi Kritsky, atcher &
Kayton, 1980), and four species occurred only in the dams
(Dactylogyridae sp. 3; Microcotyle sp.; Prosthenhystera obesa
(Diesing 1850) Travassos, 1922; and Brevimulticaecum sp.,
the latter in larval state).
Overall, Nematoda was the quantitavely predominant
group, constituting 72.5% of the parasites collected, and also
included the most prevalent species. Monogenoidea was the
most diverse group, with ten species, yet all had prevalence
lower than 10%, with the exception of Urocleidoides paradoxus
(Table 1). Digenea was the least represented group, with only
two specimens of Prosthenhystera obesa.
In the earth tanks U. paradoxus, Procamallanus
(Spirocamallanus) inopinatus, Goezia leporini and Rhabdochona
(Rhabdochona) acuminata had signicantly higher abundance,
prevalence and mean intensity of infection, and Urocleidoides
paradoxus and Urocleidoides eremitus were signicantly more
prevalent. In the dams Jainus leporini had signicantly higher
304 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
ACTA
AMAZONICA
abundance, prevalence and mean intensity of infection, and
Tereancistrum parvus showed the highest values of mean
intensity of infection (Table 2).
In the earth tanks, P. (S.) inopinatus was considered
the central species (67% prevalence), while G. leporini was
secondary (40% prevalence) and the other species were
classied as satellites (Table 2). In the dams, all ecto and
endoparasite species were classied as satellites (Table 2).
The components of the parasite community with
prevalence ≥ 10% presented an aggregated dispersion
pattern in both cultivation systems (Table 3). In the dams,
the monogenoidean J. leporini was dominant, with 88
collected specimens (44.9% of the parasites collected), the
highest value of relative dominance (0.328), and a higher
index of dispersion (ID=31.13; d=64.52). In the earth tanks,
Urocleidoides paradoxus had the highest index of dispersion
(ID=8.13; d=26.11) and G. leporini the highest value of
relative dominance (0.443).
e dominance of endoparasites was high (Table 4),
mainly owing to the relative dominance and prevalence of P.
(S.) inopinatus and G. leporini (Tables 1 and 3). Endoparasites
also had the highest index of dominance, diversity and total
evenness, while ectoparasites had the highest total richness
(Table 4). In the dams, ectoparasites were dominant, with
highest values of richness and diversity, while in the earth tanks
endoparasites had the highest indexes of richness, dominance,
diversity and evenness, while the evenness indexes of
ectoparasites were similar between the two systems (Table 4).
Discrepancy in richness and abundance of nematode species
was reected in parasite diversity, since the more abundant
communitiy determined the greatest diversity (H=3.21±0.35)
observed in the earth tanks (Table 4).
Table 1. Overall prevalence (P), mean intensity (MI), mean abundance (MA) and site of infection (SI) of parasites of Leporinus macrocephalus from cultivation
systems in Acre State, Brazil. Values for MI and MA are means ± standard deviation. Collection nr indicates the deposit code of speciemns in the helminthological
collection of Instituto Oswaldo Cruz.
Parasites Collection nr P (%) MI MA SI
MONOGENOIDEA
Dactylogyridae Bychowsky, 1933
Urocleidoides paradoxus Kritsky, Thatcher & Boeger, 1986 38674a,b; 38675, 38676, 38677 13.5 3.67 ± 2.58 0.50 ± 0.76 Gills
Urocleidoides eremitus Kritsky, Thatcher & Boeger, 1986 38678, 38679 a-c, 38680 9.5 2.11 ± 1.24 0.20 ± 0.32 Gills
Jainus leporini Abdallah, Azevedo & Luque, 2012 38672 a-b, 38673 a-c 7.0 6.93 ± 5.12 0.49 ± 0.88 Gills
Kritskyia eirasi Kritsky, Thatcher & Kayton, 1980 38670 a,b, 38671 a,b 1.0 3.00 ± 1.00 0.03 ± 0.09 Kidney
Tereancistrum parvus Kritsky, Thatcher & Kayton, 1980 38681, 38682 a,b 9.0 2.61 ± 2.30 0.23 ± 0.41 Gills
Tereancistrum paranaensis Karling, Lopes,
Takemoto & Pavanelli, 2014 38684a,b 1.5 4.33 ± 2.52 0.06 ± 0.19 Gills
Dactylogyridae sp.1 3.0 4.83 ± 2.99 0.14 ± 0.35 Gills
Dactylogyridae sp.2 1.0 1.50 ± 0.70 0.01 ± 0.05 Gills
Dactylogyridae sp.3 1.5 1.33 ± 0.57 0.02 ± 0.05 Gills
Microcotylidae Taschenberg, 1879
Microcotyle sp. * 1.0 1.0 < 0.1 Gills
DIGENEA
Callodistomidae Odhner, 1910
Prosthenhystera obesa (Diesing, 1850) Travassos, 1922 1.0 2.0 < 0.1 Gall bladder
NEMATODA
Camallanidae Railliet & Henry, 1915
Procamallanus (Spirocamallanus) inopinatus Travassos,
Artigas & Pereira, 1928 38,530-38,542 39.0 4.54 ± 3.51 1.77 ± 2.24 Intestine
Rhabdochonidae Travassos, Artigas & Pereira, 1928
Rhabdochona (Rhabdochona) acuminata (Molin, 1860) 38,543-38,544 12.0 3.42 ± 1.95 0.41 ± 0.62 Intestine
Anisakidae Railliet & Henry, 1912
Goezia leporini Martins & Yoshitoshi, 2003 38,523-38,529 21.5 10.14 ± 6.05 2.18 ± 2.93 Stomach
Acanthocheilidae Wülker, 1929
Brevimulticaecum sp. (Larva) 38,522 1.0 4.00 ± 1.41 0.04 ± 0.12 Intestine
(*) Only one individual recorded.
305 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
ACTA
AMAZONICA Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
Table 2. Prevalence, parasite abundance and mean intensity of metazoan parasites of Leporinus macrocephalus in extensive (dams) and semi-intensive (earth
tanks) cultivation systems in Acre State, Brazil. Values for abundance and intensity are means ± standard deviation. Differences between the cultivation systems
according to the Mann-Whitney test [Z(U)] were considered significant at P <0.05 (*), P <0.01 (**) and P <0.001 (***).
Prevalence (%) Parasite abundance Mean intensity
Parasites Dams Ear th tanks Z(U) Dams Ear th tanks Z (U) Dams Ear th tanks Z(U)
Urocleidoides paradoxus 11.0 16.0 1.538* 0.35±0.03 0.64±0.03 2.763*** 2.91±0.28 4.00±0.14 0.491
Urocleidoides eremitus 8.0 12.0 2.237* 0.11±0.06 0.12±0.04 1.157 1.38±0.09 2.64±0.11 1.327
Jainus leporini 11.0 3.0 2.544*** 0.88±0.05 0.09±0.21 2.088* 8.00±0.47 3.00±0.55 0.651*
Tereancistrum parvus 8.0 10.0 1.515 0.31±0.09 0.16±0.04 0.286 3.88±0.37 1.60±0.70 2.221*
Dactylogyridae sp.1 5.0 1.0 1.535 0.31±0.09 0.04±0.20 1.014 3.87±0.38 1.33±0.27 0.849
Dactylogyridae sp.2 4.0 3.0 0.437 0.07±0.06 0.05±0.01 0.966 0.80±0.05 0.71±0.04 0.480
Nematoda
Procamallanus (Spirocamallanus)
inopinatus 17.0 67.0 2.552*** 0.17±0.04 3.24±0.03 1.862* 2.80±0.11 5.00±0.05 4.184***
Rabdochona (Rabdochona)
acuminata 4.0 26.0 1.503* 0.04±0.01 0.30±0.02 3.192*** 2.00±0.25 2.75±0.06 3.020**
Goezia leporini 8.0 40.0 3.265*** 0.08±0.03 0.39±0.05 3.262*** 3.25±0.09 10.72±0.12 0.221*
Table 3. Index of dispersion (ID), d statistic and relative dominance (RD) of metazoan parasites of Leporinus macrocephalus from extensive (dams) and semi-
intensive (earth tanks) cultivation systems in Acre State, Brazil. Species with prevalence >10% are highlighted in bold. (*) Observed only in earth tanks; (**)
observed only in dams.
Dams Earth tanks
Parasites ID d RD ID d RD
Monogenoidea
Urocleidoides paradoxus 27.89 60.32 0.130 8.13 26.11 0.066
Urocleidoides eremitus - - 0.041 6.67 22.33 0.030
Jainus leporini 31.13 64.52 0.328 - - 0.009
Kritskyia eirasi* - - - - - 0.006
Tereancistrum parvus - - 0.116 3.05 3.39 0.016
Tereancistrum sp. - - - - - 0.013
Dactylogyridae sp.1 - - 0.104 - - 0.001
Dactylogyridae sp.2 - - 0.007 - - 0.001
Dactylogyridae sp.3** - - 0.015 - - -
Nematoda
Procamallanus (S.) inopinatus 7.21 23.79 0.156 4.16 6.30 0.330
Rabdochona (R.) acuminata - - 0.011 4.97 17.37 0.082
Goezia leporini - - 0.078 8.04 25.91 0.443
Brevimulticaecum sp.(larva)** - - 0.029 - - -
Total parasite abundance was signicantly correlated with
total length, weight and condition factor of the hosts in the
earth tanks, while it correlated signicantly only with total
sh length in the dams (Figure 1). ere was no signicant
dierence between parasitized and non-parasitized sh for
weight, total length and condition factor in both cultivation
systems, except for a marginally higher weight of non-
parasitized sh in the earth tanks (Table 5).
Water temperature during the time of collection was
signicantly higher in the earth tanks than in the dams (F3.92
= 7.06; p<0.001) (dams: 27.2±2.4 ºC; earth tanks: 29.1±1.6
ºC). e other measured physicochemical water parameteres
did not dier between the cultivation systems [dissolved oxygen
(dams: 6.24±1.59 mg/L; earth tanks: 6.3±1.3 mg/L); pH (dams:
6.3±0.7; earth tanks: 6.3±0.6); electrical conductivity (dams
15.89±5.46 mg/L; earth tanks: 12.33±5.55 mg/L)].
306 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
ACTA
AMAZONICA
Table 4. Richness, dominance, diversity and evenness of the parasite infracommunities of Leporinus macrocephalus from extensive (dams) and semi-intensive
(earth tanks) cultivation systems in Acre State, Brazil. Values are means ± standard deviation. Differences between cultivation systems according to the Mann-
Whitney test [Z(U)] were considered significant at P <0.05 (*), <0.01 (**) and <0.001 (***).
Ectoparasites Overall Dams Earth tanks Z(U)
Richness 2.97±1.46 2.65±0.31 2.36± 1.21 2.51**
Berger Parker dominance (d) 0.31±0.18 0.60±0.05 0.41±0.20 2.88*
Brillouin diversity (H) 1.72±0.69 1.69±0.26 1.44±0.60 4.73
Evenness (J) 0.91±0.02 0.90±0.03 0.93±0.04 3.02
Endoparasites
Richness 2.73±2.73 2.52±0.81 7.83±2.16 17.22*
Berger Parker dominance (d) 0.73±0.18 0.08±0.13 0.92±0.30 3.88***
Brillouin diversity (H) 3.34±0.37 1.43±0.47 3.21±0.35 9.31*
Evenness (J) 0.94±0.01 0.90±0.04 0.95±0.01 2.64*
Figure 1. Spearman correlation coefficient (rs) between the abundance of parasites and total length (cm), weight (g) and condition factor of Leporinus
macrocephalus in dams (A, B, C) and earth tanks (D, E, F) in Acre State, Brazil.
307 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
ACTA
AMAZONICA Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
DISCUSSION
Among the six species of Monogenoidea found
parasitizing L. macrocephalus in this study, only Microcotyle
sp. had not been already described as parasitizing other
members of the Anostomidae (Kritsky et al. 1980; Kritsky
et al. 1986; Guidelli et al. 2003; Schalch and Moraes 2005;
Guidelli et al. 2006; Takemoto et al. 2009; Takemoto and
Lizama 2010; Abdallah et al. 2012). Some ectoparasite
species that presented higher prevalence and abundance
may have specicity to members of Anostomidae, such as U.
paradoxus and T. parvus (Cohen et al. 2013). In the upper
Parana River oodplain, U. paradoxus parasitized Leporinus
lacustris and L. friderici with respective prevalences of 32%
and 46.1%, while Jainus spp. was the monogenoidean with
higher prevalence, abundance and mean intensity in both
host species (Guidelli et al. 2006). Similarly, in our study J.
leporini was the monogenoid with the highest values of all
parasitic indexes, except prevalence, in the dams.
e prevalence of parasites in the earth tanks in our study
was similar to the prevalence reported for L. macrocephalus in
sh farms in southeastern Brazil (65%, Martins and Yoshitoshi
2003, and 87%, Moraes 2005). e generally higher indices of
parasite prevalence, abundance and mean infection intensity
observed in the earth tanks in comparison to the dams, can
be explained by the higher density of sh in the earth tanks,
which favors the dissemination of infectious forms of parasites
(Sanches 2008).
The higher water temperature in the earth tanks, as
compared to the dams, may also have contributed to the
multiplication of parasites, reecting in higher abundance and
infection intensity. Water temperature is one of the key abiotic
environmental factors controlling parasite dynamics in aquatic
systems, which may directly inuence the rates of parasite
establishment, development and release of infective stages,
as well as parasite transmission between hosts (Karvonen et
al. 2013).
Prosthenhystera obesa was found parasitizing the gall bladder
of the host. is parasite is relatively large in comparison with
the size of the parasitized organ. e low prevalence of Digenea
in the dams and their absence in the earth tanks was probably
due to a reduced presence of their intermediate hosts. e
application of calcium oxide in the surroundings of dams
and earth tanks is common, which causes a reduction in the
population of snails, which are intermediate hosts for these
helminthes. In addition, sh farmers undertake the control of
aquatic plants, thus minimizing the amount of organic waste
that serves as mollusc feed.
Although the same nematode species were found in both
cultivation systems (with the exception of Brevimulticaecum
sp. larvae in the dams), only in the earth tanks they constituted
the main component of the parasite community of L.
macrocephalus. Among Nematoda, P. (S.) inopinatus had the
highest prevalence and parasite abundance indexes. Several
studies recorded an increase in the prevalence of this species
in other neotropical sh, both in natural environments and
in cultivation systems (Andrade and Malta 2006; Saraiva
et al. 2006; Araújo et al. 2009; Gomiero et al. 2009).
Procamallanus (S.) inopinatus was the most prevalent parasite
species of Leporinus lacustris and L. friderici in the Nova
Ponte Reservoir, in southeastern Brazil (Feltran et al. 2004).
In the upper Parana River oodplain, in southern Brazil, the
parasite had a prevalence of 20.6% in L. lacustris and 29.8%
in L. friderici (Guidelli et al. 2006). e present study reports
the rst quantitative data for P. (S.) inopinatus parasitizing
L. macrocephalus. Goezia leporini is known to parasitize
L. macrocephalus in cultivation systems in São Paulo, in
southeastern Brazil (Martins and Yoshitoshi 2003).
In this study, G. leporini did not show the clinical signs
of disease reported by Martins and Yoshitoshi (2003).
However, some specimens of G. leporini were attached to the
gastric tract of the hosts, causing bleeding and gastric ulcers,
which were reported as secondary lesions from this parasite’s
infection (Deardor and Overstreet 1980). Although G.
leporini in this study had the highest mean intensity of
Table 5. Weight (g), total length (cm) and condition factor of Leporinus macrocephalus in extensive (dams) and semi-intensive (earth tanks) cultivation systems
in Acre State, Brazil. Values are means ± standard deviation. Differences between the cultivation systems according to the t-test were considered significant
at P <0.05 (*).
Parameter
Dams
t
Earth tanks
t
Parasitized Non-parasitized Parasitized Non-parasitized
Weight 286.70±62.76 290.65±64.27 1.48 339.80±71.89 346.02±82.27 3.54*
Total length 27.16±1.66 28.59±2.49 1.17 28.33±2.27 29.26±1.89 1.26
Condition factor 0.92±0.13 0.95±0.17 1.69 0.94±0.15 0.96±0.19 1.33
308 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
ACTA
AMAZONICA
infection in both systems (10.1), they had low prevalence
(21.5%), while in southeastern Brazil prevalence was higher
(65%), with lower mean infection intensity (4.1) (Martins
and Yoshitoshi 2003).
e aggregated dispersion of metazoan parasites in L.
macrocephalus found in our study is a common pattern in
parasite communities of freshwater sh in dierent regions
of Brazil (Machado et al. 1996; Abdallah et al. 2004; Moreira
et al. 2005; Paraguassú and Luque 2007; Guidelli et al. 2009;
Neves et al. 2013; Tavares-Dias et al. 2013). is mode of
dispersion has been associated with the direct life cycle of
Monogenoidea parasites, as well as the susceptibility and
capacity of immunological response of the hosts (Paraguassú
and Luque 2007; Tavares-Dias et al. 2013). Dispersion
values were lower for species with high prevalence, because
aggregation tends to decrease as the proportion of hosts that
are infected increases, and parasites spread more evenly among
hosts, leaving fewer hosts uninfected (Poulin 1993).
e signicant positive correlation of parasite abundance
with total host length was expected since fish length is
positively correlated with age, and thus larger specimens had
more contact time with the infecting forms and, consequently,
a greater accumulation of parasites (Luque and Chaves 1999).
However, the parasitism does not necessarily increase in larger
sh as a function of mechanical accumulation over a longer
exposure time. For example, in Monogenoidea the positive
correlation of parasite abundance with sh weight and length
is likely facilitated by larger gills in larger sh, which provides
more space for parasite attachment (Luque and Chaves 1999;
Azevedo et al. 2007).
CONCLUSIONS
is is the rst study of parasites in cultivated Leporinus
macrocephalus in the state of Acre, Brazil, increasing the
knowledge of the biodiversity and ecological descriptors of
the parasite communities of this sh species in the Amazon
region. Our results indicate that the parasite fauna of L.
macrocephalus in extensive and semi-intensive cultivation
systems in Acre does not dier very signicantly. Parasitic
indexes were low and varied among species, with the highest
values in quantitative and ecological parasitism descriptors
for Monogenoidea in the extensive, and Nematoda in the
semi-intensive system. Although clinical signs of disease
were not observed, parasite data suggest that prophylactic
measures against future epizootic outbreaks may be indicated
to avoid economic losses in sh farming due to parasitism.
e occurrence of adult species of Nematoda indicated the
availability of the intermediate hosts of these helminths and
brings to attention the necessity of adequate sanitary control
in sh farms.
ACKNOWLEDGEMENT
e study was nancially supported by the Oswaldo
Cruz Institute (Rio de Janeiro) and the Federal Institute of
Acre (IFAC).
REFERENCES
Abdallah, V.D.; Azevedo, R.K de; Luque, J.L. 2012. ree new
species of Monogenea (Platyhelminthes) parasites of sh in the
Guandu river, southeastern Brazil. Acta Scientiarum. Biological
Sciences, 34: 483-490.
Abdallah, V.D.; Azevedo, R.K.; Luque, J.L. 2004. Metazoários
parasitos dos lambaris Astyanax bimaculatus (Linnaeus, 1758),
A. parahybae Eigenman, 1908 e Oligosarcus hepsetus (Cuvier,
1829) (Osteichthyes: Characidae), do Rio Guandu, Estado do
Rio de Janeiro, Brasil. Brazilian Journal of Veterinary Parasitology,
13: 57-63.
Andrade, S.M.S.; Malta, J.C.O. 2006. Fauna monitoring of Matrinxã
Brycon amazonicus (Spix & Agassiz, 1829) raised in an intensive
husbandry system in a stream channel in the state of Amazonas.
Brazilian Journal of Biology, 66: 1123-1132.
Andrian, I.D.F.; Dória, C.D.C.Torrente, G.; Ferretti, C.M.L. 1994.
Espectro alimentar e similaridade na composição da dieta de
quatro espécies de Leporinus (Characiformes, Anostomidae) do
Rio Paraná, Brasil. Revista Unimar, 16: 97-106.
Araújo, C.S.O.; Gomes, A.; Tavares, D.M.; Andrade, S.M.S.; Belem,
A.C.; Borges, T.B.M. 2009. Parasitic infections in pirarucu
fry, Arapaima gigas Shinz, 1822 (Arapaimidae) kept in a semi-
intensive sh farm in Central Amazon, Brazil. Journal of the
Faculty of veterinary Medicine University of Zagreb, 79: 499-507.
Azevedo, G.B.; Madi, R.R.; Ueta, M.T. 2007. Metazoans parasites
of Astyanax altiparanae (Pisces: Characidae) at Rio das Pedras
Farm, Campinas, SP, Brazil. Bioikos, 21: 89-96.
Bush, A.O.; Holmes, J.C. 1986. Intestinal helminths of lesser scaup
ducks: an interactive community. Canadian Journal of Zoology,
64: 142-152.
Bush, A.O.; Lafferty, K.D.; Lotz, J.M.; Shostak, A.W. 1997.
Parasitology meets ecology on its own terms. Journal of
Parasitology, 83: 575-583.
Cohen, S.C.; Justo, M.C.N.; Kohn, A. 2013. South American
Monogenoidea parasites of shes, amphibians and reptiles. 1st ed.
Ocina de Livros, Rio de Janeiro, 663p.
Deardor, T.I.; Overstreet, R.M. 1980. Taxonomy and biology of
North American species of Goezia (Nematoda: Anisakidae) from
shes, including three news species. Proceeding Helminthology
Society of Washington, 47: 192-217.
Feltran, R. de B., Marçal Júnior, O., Pinese, J.F., Takemoto, R.M.
2004. Prevalência, abundância, intensidade e amplitude de
infecção de nematóides intestinais em Leporinus friderici
(Bloch, 1794) e L. obtusidens (Valenciennes, 1836) (Pisces,
Anostomidae), na represa de Nova Ponte (Perdizes, MG). Revista
Brasileira de Zoociência, 6: 169-179.
309 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
ACTA
AMAZONICA Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
Gomiero, L.M.; Villares, J.G.A.; Naous, F. 2009. Reproduction of
Cichla kelberi Kullander and Ferreira, 2006 introduced into an
articial lake in southeastern Brazil. Brazilian Journal of Biology,
69: 175-183.
Guidelli, G.M.; Isaac, A.; Takemoto, R.M.; Pavanelli, G.C. 2003.
Endoparasite infracommunities of Hemisorubim platyrhynchos
(Valenciennes, 1840) (Pisces: Pimelodidae) of the Baía river,
upper Paraná river oodplain, Brazil: specic composition and
ecological aspects. Brazilian Journal of Biolology, 63: 261-268.
Guidelli, G.; Tavechio, W.L.G.; Takemoto, R.M.; Pavanelli, G.C.
2006. Fauna parasitária de parasitária de Leporinus lacustres e
Leporinus friderici (Characiformes, Anostomidae) da planície de
inundação do alto rio Paraná, Brasil. Acta Scientiarum Biological
Sciences, 3: 281-290.
Guidelli, G.; Takemoto, R.M.; Pavanelli, G.C. 2009. Ecology of the
ectoparasite infrapopulations in the nasal cavities of Leporinus
lacustris (Anostomidae) from the upper Paraná river oodplain,
Brazil. Acta Scientiarum. Biological Sciences, 31: 209-214.
Karvonen, A.; Kristjánsson, B.K.; Skúlason, S.; Lanki, M.; Rellstab,
C. Jokela, J. 2013. Water temperature, not fish morph,
determines parasite infections of sympatric Icelandic threespine
sticklebacks (Gasterosteus aculeatus).Ecology and Evolution: 3:
1507-1517.
Kritsky, D.C.; atcher, V.E.; Boeger, W.A. 1986. Neotropical
Monogenea. Revision of Urocleidoides (Dactylogyridae,
Ancyrocephalinae). Proceedings of the Helminthological Society
of Washington, 53: 1-37.
Kritsky, D.C.; atcher, V.E.; Kayton, R.J. 1980. Neotropical
Monogenea. Five new species from South America with the
proposal of Tereancistrum gen. n. and Trinibaculum gen. n.
(Dactylogyridae: Ancyrocephalinae). Acta Amazonica, 10:
411-417.
Le Cren, E.D. 1951. e length-weight relationship and seasonal
cycle in gonad weight and condition in the perch (Perca
uviatilis). Journal Animal Ecology, 20: 201-219.
Luque, J.L.; Chaves, N.D. 1999. Ecologia da comunidade de
metazoários parasitos da anchova Pomatomus saltator (Linnaeus)
(Osteichthyes, Pomatomidae) do litoral do estado do Rio de
Janeiro, Brasil. Revista Brasileira de Zoologia, 16: 711-723.
Machado, M.H.; Pavanelli, G.C.; Takemoto, R.M. 1996. Structure
and diversity of endoparasitic infracommunities and the
trophic level of Psedoplatystoma corruscans and Schizodon borelli
(Osteichthyes) of the high Paraná River. Memórias do Instituto
Oswaldo Cruz, 91: 441- 448.
Magurran, A.E. 2004. Measuring biological diversity. 1st ed. Blackwell
Publishing, Oxford. 264p.
Martins, M.L.; Tavares-Dias, M.; Fujimoto, R.Y. Onaka, E.M.;
Nomura, D.T. 2004 Haematological alterations of Leporinus
macrocephalus (Osteichtyes: Anostomidae) naturally infected by
Goezia leporini (Nematoda: Anisakidae) in sh pond. Arquivo
Brasileiro de Medicina Veterinária e Zootecnia. 56: 640-646.
Martins, M.L.; Yoshitoshi, E.R. 2003. A new nematode species
Goezia leporini n. sp. (Ascaridoidea) from cultivated freshwater
sh Leporinus macrocephalus (Anostomidae) in Brazil. Brazilian
Journal of Biolology, 63: 497-506.
Moreira, S.T.; Ito, K.F.; Takemoto, R.M.; Pavanelli, G.C. 2005.
Ecological aspects of the parasites of Iheringichthys labrosus
(Lütken, 1874) (Siluriformes: Pimelodidae) in reservoirs
of Paraná basin and upper Paraná floodplain, Brazil. Acta
Scientiarum. Biological Sciences, 27: 317-322.
Neves, L.R.; Pereira, F.B.; Tavares-Dias, M.; Luque, J.L. 2013.
Seasonal inuence on the parasite fauna of a wild population of
Astronotus ocellatus (Perciformes: Cichlidae) from the Brazilian
Amazon. e Journal of Parasitology, 99: 718-721.
Paraguassú, A.R.; Luque, J.L. 2007. Metazoários parasitos de seis
espécies de peixes do reservatório de Lajes, Estado do Rio de
Janeiro, Brasil. Brazilian Journal of Veterinary Parasitology, 16:
121-128.
Pavanelli, G.C.; Takemoto, R.M. Eiras, J. da C. 2013. Parasitologia
de Peixes de água doce do Brasil. 1st ed. Eduem, Maringá, 452p.
Poulin, R. 1993. e disparity between observed and uniform
distributions: a new look at parasite aggregation. International
Journal of Parasitology, 23: 937-944.
Rohde, K.; Hayward, C.; Heap, M. 1995. Aspects of the ecology of
metazoan ectoparasites of marine shes. International Journal
for Parasitology, 25: 945-970.
Rózsa, L., Reiczigel, J., Majoros, G. 2000. Quantifying parasites
in samples of hosts. e Journal of Parasitology, 86: 228-232.
Sanches EG. Controle de Neobenedenia melleni (Maccallum, 1927)
(Monogenea: Capsalidae) em Garoupa-Verdadeira, Epinephelus
marginatus (Lowe, 1834), cultivada em tanques-rede. 2008.
Revista Brasileira de Parasitologia Veterinária, 17: 145-149.
Saraiva, A.; Silva, F.A.; Silva, A.T. 2006. Parasites of the characid
sh Brycon hilarii from the River Juba, Mato Grosso, Brazil.
Helminthologia, 43: 158-160.
Schalch, S.H.; Moraes, F.R. 2005. Distribuição sazonal de parasitos
branquiais em diferentes espécies de peixes em pesque-pague do
município de Guariba-SP, Brasil. Brazilian Journal of Veterinary
Parasitology, 14: 141-146.
Soares Junior, M.S.; Caliari, M.; Pereira, D.E.P. 2013. Eect of
soybean inclusion in extruded rations on performance of juvenile
Piavuçu (Leporinus macrocephalus L.). Ciência Animal Brasileira,
14: 399-405.
Takahashi, L.S.; Gonçalves, F.D.; Abreu, J.S.D.; Martins, M.I.E.G.;
Ferreira, A.C.M. 2004. Economic viability of the piauçu
Leporinus macrocephalus (Garavello & Britski, 1988) production.
Scientia Agricola, 61: 228-233.
Takemoto, R.M.; Lizama, M.L.A.P. 2010. Helminth fauna of
shes from the upper Paraná rive oodplain, Brazil. Neotropical
Helminthology, 4: 5-8.
Takemoto, R.M.; Pavanelli, G.C.; Lizama, M.A.P.; Lacerda, A.C.F;
Yamada, F.H., Moreira, L.H.A.; Ceschini, T.L.; Bellay, S. 2009.
Diversity of parasites of sh from the Upper Paraná River
oodplain, Brazil. Brazilian Journal Biolology, 69: 691-705.
310 VOL. 47(4) 2017: 301 - 310 MARTINS et al.
Metazoan parasite communities of Leporinus macrocephalus (Characiformes: Anostomidae)
in cultivation systems in the western Amazon, Brazil
ACTA
AMAZONICA
Tavares-Dias, M.; Neves, L.R.; Pinheiro, D.A.; Oliveira, M.S.B.;
Marinho, R.G.B. 2013. Parasites in Curimata cyprinoides
(Characiformes: Curimatidae) from eastern Amazon, Brazil.
Acta Scientiarum Biological Sciences, 35: 595-601.
Tavares-Dias, M.; Schalch, S.H.; Martins, M.L.; Silva, E.S. F.;
Moraes, R.; Perecin, D. 1999. Hematologia de teleósteos
brasileiros com infecção parasitária. I. Variáveis do Leporinus
macrocephalus Garavelo & Britski, 1988 (Anostomidae) e
Piaractus mesopotamicus Holmberg, 1887 (Characidae). Acta
Scientiarum, 21: 337-342.
Zago, A.C.; Franceschini, L.; Garcia, F.; Schalch, S.H.C.; Gozi, K.S.;
Silva, R.J. da. 2014. Ectoparasites of Nile tilapia (Oreochromis
niloticus) in cage farming in a hydroelectric reservoir in Brazil.
Brazilian Journal of Veterinary Parasitology, 23: 171-178.
Zanolo, R.; Yamamura, M.H. 2006. Parasitas em tilápias-do-nilo
criadas em sistema de tanques-rede. Semina, 27: 281-288.
Zar, J.H. 2010. Biostatistical analysis. 5th ed. Prentice Hall, New
Jersey, 662p.
Received: 25/04/2017
Accepted: 23/07/2017
