ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2018, 12(2), jul-dic:141-146.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
METAZOAN PARASITES OF SERRASALMUS ALTISPINIS (SERRASALMIDAE) FROM
FLOODPLAIN LAKES OF THE BRAZILIAN AMAZON
METAZOÁRIOS PARÁSITOS DE SERRASALMUS ALTISPINIS (SERRASALMIDAE) DE LAGOS
INUNDABLES DE LA AMAZONÍA BRASILEÑA
1Instituto de Investigaciones de la Amazonía Peruana. Centro de Investigaciones Fernando Alcántara (CIFAB - IIAP).
Laboratorio de Parasitología y Sanidad Acuícola. Carretera Iquitos-Nauta, Km. 4.5, San Juan Bautista, Iquitos – Perú.
2Instituto Nacional de Pesquisas da Amazônia (INPA, Manaus, Brasil). Av. André Araújo, 2936 – Petrópolis, Manaus,
Amazonas, Brasil 69067-375. Programa de Pós-graduação em Biología de Água Doce e Pesca Interior-BADPI
*Corresponding author: E-mail: germantiss1106@gmail.com
1,* 2
Germán Augusto Murrieta Morey & José Celso de Oliveira Malta
ABSTRACT
Keywords: Amazon – ectoparasites – endoparasites – parasitological indices – piranha – Serrasalmus altispinis
This work describes the parasitic fauna of Serrasalmus altispinis Merckx, Jégu and Santos, 2000 caught in
floodplain lakes of the Brazilian Amazon. All parasite species reported represent first records for this host.
The studied lakes were: Baixio, Preto, São Tomé, Ananá, Araçá and Maracá, located between the cities of
Manaus and Coari in Central Amazonia. Sixty S. altispinis were collected and examined in March, June,
September, and December 2013. Thirty-six species belonging to Monogenoidea, Digenea, Nematoda,
Copepoda, Branchiura and Isopoda were identified. Parasitological indices obtained in this study indicate
that the community of endoparasites of S. altispinis is characterized by low prevalence, low number of
individuals and low number of species. In contrast, ectoparasites presented higher prevalence and higher
number of individuals and species.
Neotropical Helminthology
141
Volume12,Number2(jul-dec2018)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
RESUMEN
Palabras clave: Amazonas – ectoparásitos – endoparásitos – índices parasitarios – piraña – Serrasalmus altispinis
Este trabajo describe la fauna parasitaria de Serrasalmus altispinis Merckx, Jégu y Santos, 2000
provenientes de lagos inundables de la Amazonía brasileña. Todas las especies identificadas representan
los primeros registros para este hospedero. Los lagos estudiados fueron: Baixio, Preto, São Tomé, Ananá,
Araçá y Maracá, localizados entre las ciudades de Manaus y Coari en la Amazonía Central. Sesenta S.
altispinis fueron colectados y examinados durante cuatro expediciones en Marzo, Junio, Septiembre y
Diciembre del 2013. Fueron identificadas 36 especies pertenecientes a Monogenoidea, Digenea,
Nematoda, Copepoda, Branchiura e Isopoda. Los índices parasitológicos obtenidos en este estudio
indican que la comunidad de endoparásitos de S. altispinis es caracterizada por baja prevalencia, bajo
número de individuos y bajo número de especies. En contraste, los ectoparásitos presentan alta
prevalencia y un alto número de individuos y especies.
142
Neotropical Helminthology, 2018, 12(2), jul-dic
INTRODUCTION the Purus River (03°49' 39,0"S/ 61°25' 24,6" W).
Fish were caught using 100 mm between adjacent
nodes-meshed, 20 m long x 2 m high gillnets.
Posteriorly the fishes were quickly immersed in 75
mg clove oil L solution and euthanized
-1
·
(CONCEA, 2013). In the field, fishes were
measured and weighed. The gills, operculum and
fins were examined for the presence of
ectoparasites. Gills and nostrils were removed and
preserved 5% formalin; the gastrointestinal tract
was preserved in 70% ethanol for posterior
analyses at the laboratory of Fish Parasitology
(LPP) in the National Institute of Amazonian
Research (INPA), Manaus, Brazil.
At the laboratory, the parasites found were
processed according to Amato et al. (1991).
Specimens were studied using a light microscope
Zeiss Axioscope 2. Voucher specimens were
deposited at the invertebrate collection of the
National Institute of Amazon Research (INPA),
Manaus, Brazil. The ecological terminology
applied to parasites followed Bush et al. (1997).
All specimens of S. altispinis were parasitized by at
least one parasite species. There were found 1,122
specimens of parasites. We identified 36 species,
23 belonging to Monogenoidea, 1 to Digenea, 5 to
Nematoda, 4 to Copepoda, 1 to Branchiura and 2 to
Isopoda (Table 1).
The highest prevalence of infection was 50% for
Anacanthorus jegui Van Every & Kritsky, 1992,
the highest mean intensity and mean abundance of
infection was found for Amplexibranchius
bryconis Thatcher & Paredes, 1995 (Table 1).
In this study S. altispinis was parasitized by 23
species of Monogenoidea from eight genera.
Species allocated in five of these genera are
specific of Serrasalmidae namely: Amphithecium;
Within Serralsamidae, Serrasalmus altispinis
Merckx, Jégu & Santos, 2000, commonly known
as “piranha seca” can reach 19 cm and inhabits
lakes of white water rivers, being usually captured
near to the aquatic vegetation and in flooded forest
(Claro-Jr., 2003). According to Claro-Jr. (2003) S.
altispinis feeds on scales and fins of fishes and can
also swallow small fishes and invertebrates.
Taxonomic studies that discover new species, new
host and geographical occurrences represent
enormous contribution to the knowledge of the
biodiversity of a determinate area and constitute a
base for other studies in parasitological ecology,
environmental impacts, biotic integrity and
conservation of ecosystems (Luque & Poulin,
2007). Studies on parasite communities and
diversity in fish from the Amazon increase the
knowledge of the richness and diversity in this
ecosystem.
For S. altispinis there is still scarce information on
their parasitic fauna. The only records for this
species are cited by Oliveira et al. (2017) who
found the crustaceans Braga patagonica Schiodte
& Meinert, 1884 on the mouth and Argulus
nattereri Heller, 1857 on the integument of
specimens collected in the state of Amapá, Brazil.
The parasitic fauna of S. altispinis has been poorly
studied. Thus, the objective of the present study
was to identify the metazoan parasite fauna of S.
altispinis collected in different floodplain lakes
from the Brazilian Amazon.
Between March and December 2013, 60 S.
altispinis (Figure 1) were caught in six floodplain
lakes of the Solimões River: Lake Baixio
(03°17'27, 2''S/ 60°04'29,6''W) at the city of
Iranduba, Lake Preto (03°21'17, 1''S/
60°37'28,6''W) at Manacapurú; Lake Ananá
(03°53'54,8''S/ 61°40'18,4''W) at Anori; Lake
Araçá (S03°45' 04,3" S/ 62°21' 25,9" W) at
Codajás and Lake Maracá (03°50'32,8''S/
62°34'32,4''W) at Coari and Lake São Tomé at the
Murrieta Morey & Oliveira Malta
MATERIAL AND METHODS
RESULTS
DISCUSSION
143
Parasites
Accession No
P%
N
mI
mA
MONOGENOIDEA
Amphithecium diclonophallum Kritsky, Boeger & Jégu, 1997
INPA 622
11.67
12
1.71 ± 1.49
0.20
Amphithecium falcatum Boeger & Kritsky, 1988
INPA 623
36.67
71
3.22 ± 3
1.18
Anacanthorus amazonicus Kritsky & Boeger
1995
INPA 624
13.33
21
2.62 ± 4.20
0.35
Anacanthorus cintus Van Every & Kritsky, 1992
INPA 625
3.33
4
2 ± 1.41
0.07
Anacanthorus cladophallus Van Every & Kritsky, 1992
INPA 626
1.67
1
1
0.02
Anacanthorus crytocaulus Van Every & Kritsky, 1992
INPA 627
3.33
2
1
0.03
Anacanthorus gravihamulatus Van Every & Kritsky, 1992
INPA 628
3.33
2
1
0.03
Anacanthorus jegui Van Every & Kritsky, 1992
INPA 629
50.00
104
3.46 ± 2.99
1.73
Anacanthorus lepyrophallus Kritsky, Boeger & Van Every 1992
INPA 630
21.67
45
3.46 ± 4.99
0.75
Anacanthorus mesocondylus Van Every & Kritsky, 1992
INPA 631
30.00
34
1.88 ± 2.80
0.57
Anacanthorus peryphallus Kritsky, Boeger & Van Every 1992
INPA 632
21.67
21
1.61 ± 0.76
0.35
Anacanthorus prodigiosus Van Every & Kritsky, 1992
INPA 633
15.00
12
1.33 ± 0.70
0.20
Anacanthorus sciponophallus Van Every & Kritsky, 1992
INPA 634
33.33
44
2.2 ± 1.63
0.73
Anacanthorus serrasalmi Van Every & Kritsky, 1992
INPA 635
5.00
4
1.33 ± 0.57
0.07
Ancanthorus sp.
INPA 636
36.67
68
3.04 ± 1.60
1.13
Calpidothecium crescentis Mizelle & Price, 1965
INPA 635
1.67
1
1
0.02
Enallothecium aegidatum Kritsky, Boeger & Jégu, 1998
INPA 636
26.67
54
3.31 ± 1.92
0.90
Myramothecium whittingtoni Kritsky, Boeger & Jégu, 1996
INPA 637
3.33
2
1
0.03
Notothecium cyphophallum Kritsky, Boeger & Jegú, 1998
INPA 638
28.33
71
4.17 ± 5.99
1.18
Notothecium deleastoideum Kritsky, Boeger & Jegú, 1998
INPA 639
38.33
149
6.43 ± 6.05
2.48
Notozothecium euzeti Kritsky, Boeger & Jegú, 1996
INPA 640
1.67
1
1
0.02
Notozothecium minor Boeger & Kritsky, 1988
INPA 641
20.00
16
1.33 ± 0.77
0.27
Rhinoxenus piranhus Kritsky, Boeger & Thatcher, 1988
INPA 642
35.00
78
3.71 ± 4.05
1.30
DIGENEA
Clinostomum marginatum (Rudolphi, 1819)
INPA 689 a -b
16.67
22
2.2 ± 3.15
0.37
NEMATODA
Procamallanus
(Spirocamallanus)
inopinatus
Travassos, Artigas & Pereira, 1928
INPA 79, 80
55.00
48
1.45 ± 1
0.8
Anisakis sp.
INPA 77, 78
11.67
13
1.86 ± 1.9
0.21
Contracaecum sp.
INPA 83
1.67
2
2
0.03
Pseudoproleptus sp.
INPA 82
3.33
6
3
0.1
Philometra nattereri Cárdenas, Moravec, Fernándes & Morais 2011
INPA 81
1.67
1
1 ± 2.82
0.01
COPEPODA
Amplexibranchius bryconis Thatcher & Paredes, 1995
INPA 2236
35.00
163
7.8 ± 2.82
2.72
Ergasilus jaraquensis Thatcher & Robertson, 1982
INPA 2235
17.00
10
1 ± 0.5
0.17
Gamidactylus jaraquensis Thatcher & Boeger, 1984
INPA 2234
17.00
22
2.2 ± 1.5
0.4
Rhinergasilus piranhus Boeger & Thatcher, 1988
INPA 2233
1.67
1
1
0.02
BRANCHIURA
Argulus chicomendesi Malta & Varella, 2000
INPA 2231
1.67
1
1
4.4
ISOPODA
Amphira branchialis Thatcher, 1993
INPA 2229
11.67
14
2
0.23
Vanamea symetrica (Van Name, 1925) INPA 2230 1.67 1 1 0.02
Table 1. Metazoan parasites in Serrasalmus altispinis Merckx, Jégu and Santos, 2000 from Brazilian Amazon
floodplain lakes. P% = prevalence, N = number of parasites, mI = mean intensity, mA = mean abundance.
Metazoan parasites of Serrasalmus altispinis
Neotropical Helminthology, 2018, 12(2), jul-dic
144
Figure 1. Lateral view of Serrasalmus altispinis Merckx, Jégu and Santos, 2000 captured in floodplain lakes of the Brazilian
Amazon.
Calpidothecium; Enallothecium; Myramothecium
and Notothecium. Three genera are not host
specific namely: Anacanthorus, which also
parasitizes fish species of Characidae and
Curimatidae, Notozothecium that is also found in
Cynodontidae and Rhinoxenus that parasitizes
Characidae (Braga e t a l . , 2014). All
monogenoideans recorded in the present study are
first records for S. altispinis.
In floodplain lakes from the Brazilian Amazon,
Clinostomum marginatum was recorded infecting
the gills of Cichla monoculus Spix & Agassiz, 1831
(Paredio, 2014), in the musculature of Pygocentrus
nattereri Kner, 1858 (Morais, 2011), and in gills,
eyes, intestine and liver of Acestrorhynchus
falcirostris (Cuvier, 1819) (Dumbo, 2014). In the
present study, C. marginatum is cited for the first
time parasitizing S. altispinis. This parasite is
capable to parasitize different organs of several fish
species in floodplain lakes of the Brazilian
Amazon.
In floodplain lakes of the Brazilian Amazon,
Anisakis sp., Pseudoproleptus sp. and P. (S.)
inopinatus were found parasitizing the intestine,
stomach and liver of P. nattereri (Morais, 2011)
and A. falcirostris (Dumbo, 2014). Morais (2011)
cited Philometra nattereri parasitizing the eyes of
P. nattereri. Dumbo (2014) found Contracaecum
sp. parasitizing the intestine and stomach of A.
falcirostris. In the present study, all these
nematodes are cited for the first time in S.
altispinis, expanding the number of known hosts
for these parasites.
Amplexibranchius bryconis was cited for the first
time in Brazil parasitizing the gills of Potamorhina
latior (Spix & Agassiz, 1829) captured in
floodplain lakes of the Brazilian Amazon (Morey
et al., 2015). The second record was reported in A.
falcirostris captured in the same lakes (Dumbo,
2014). In the present study, this copepod species is
cited for the third time in Brazil, parasitizing a new
host, representing the first record for S. altispinis.
Ergasilus jaraquensis was found for the first time
parasitizing the gills of Semaprochilodus insignis
(Jardine, 1841) collected in the River Solimões
(Thatcher & Robertson, 1982). In floodplain lakes
of the Brazilian Amazon, E. jaraquensis was cited
parasitizing P. latior (Morey et al., 2015). In the
Neotropical Helminthology, 2018, 12(2), jul-dic Murrieta Morey & Oliveira Malta
Amato, JFR, Boeger, WA & Amato, SB. 1991.
Protocolos para laboratório coleta e
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Imprensa Universitária, Universidade
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Bellay, S, Oliveira, EF, Almeida-Neto, M, Lima
Junior, DP, Takemoto, RM & Luque, JL.
2013. Developmental stages of parasites
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Braga, MP, Araújo, SB & Boeger, WA. 2014.
Patterns of interaction between Neotropical
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Mon o ge noid e a ( P l at yhel m in th es).
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Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.
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own terms: Margolis et al. revisited. The
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583.
Claro Jr, LH. 2003. A influência da floresta
alagada n a estrutu r a trófic a de
comunidades de peixes em lagos de várzea
da Amazônia Central. Tesis de mestrado.
INPA-UFAM, Manaus, 61 pp.
Carvalho, LN, Arruda, R & Del-Claro, K. 2004.
Host-parasite interactions between the
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Dumbo, JC. 2014. Espécies de metazoários
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Lacerda, ACF, Takemoto, RM, Lizama, M &
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145
present study, S. altispinis is cited as a new host for
this parasite species.
In floodplain lakes of the Brazilian Amazon,
Rhinergasilus piranhus was found in the nostrils of
P. nattereri (Morais, 2011). According to Varella &
Malta (1995), R. piranhus is usually found together
with Gamidactylus jaraquensis. These two
copepods were also collected in the nostrils of
different fish species from the River Paraná
(Lacerda et al., 2008). In the present study, R.
piranhus and G. jaraquensis were found in the
nostrils of S. altispinis, being new records for this
fish.
The branchiuran Argulus chicomendesi was found
parasitizing the body surface of P. nattereri
collected in floodplain lakes of the Brazilian
Amazon (Morais, 2011). In the present study, only
one specimen of A. chicomendesi was found in S.
altispinis. However, it represents the first record of
this parasite in this host; it may also be considered
as an accidental infestation.
For Serrasalmidae, the isopod Anphira branchialis
was cited parasitizing P. nattereri (Thatcher, 1993;
Carvalho et al., 2004; Vital et al., 2011; Morais,
2011; Tavares-Dias et al., 2015), Serrasalmus
spilopleura Kner, 1858 Serrasalmus sp. (Thatcher,
1993; Tavares-Dias et al., 2015). Vanamea
symetrica was cited parasitizing S. elongatus Kner,
1858, S. rhombeus (Linnaeus, 1766), S. spilopleura
and Serrasalmus sp. (Thatcher, 1993). In the
present study, these two isopods are cited for the
first time in S. altispinis.
The presence of parasites in larval stage indicates
that a fish species is a prey with an intermediate
position in the food chain and is an intermediate or
paratenic host of one or more parasite species
(Bellay et al., 2013, Poulin & Leung 2011). In the
present study two endoparasite species were found
in adult stage and four were found in larval stage,
indicating that S. altispinis is a definitive host of P.
(S.) inopinatus and Philometra nattereri Cardenas,
Movarec, Fernandes & Morais, 2012 and
intermediate or paratenic host of C. marginatum,
A n i s a k i s s p , C o n t r a c a e c u m s p a n d
Pseudoproleptus sp. This fish occupies an
intermediate position in the food web, feeding on
other organisms and being predated by other
vertebrates.
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Neotropical Helminthology, 2018, 12(2), jul-dic Murrieta Morey & Oliveira Malta
