ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
RESEARCH NOTE / NOTA CIENTÍFICA
FIRST RECORD IN BRAZIL OF AN ERGASILUS SPECIES (CYCLOPOIDA: ERGASILIDAE)
PARASITIZING THE GILLS AND NASAL FOSSAE OF RAPHIODON VULPINUS
(CHARACIFORMES: CYNODONTIDAE)
PRIMER REGISTRO EN BRASIL DE UNA ESPECIE DE ERGASILUS (CICLOPOIDA:
ERGASILIDAE) PARASITANDO LAS BRANQUIAS Y FOSAS NASALES DE RAPHIODON
VULPINUS (CHARACIFORMES: CYNODONTIDAE)
1 Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo, 2936 – Petrópolis, Manaus, Amazonas, Brazil
69067-375. Programa de Pós-graduação em Biología de Água Doce e Pesca Interior-BADPI. germantiss1106@gmail.com
2 Instituto Nacional de Pesquisas da Amazônia (INPA), Coordenação de Biodiversidade, Laboratório de Parasitologia e
Patologia de Peixes, Av. André Araújo, 2936 – Petrópolis, Manaus, Amazonas, Brazil 69067-375. angelvarella1@gmail.com;
jcmalta@inpa.gov.br
1 2 2
Germán Augusto Murrieta Morey , Angela Maria Bezerra Valera & José Celso de Oliveira Malta
ABSTRACT
Key words: Copepoda – floodplain lakes – parasite – Raphiodon vulpinus
Ergasilid species are found parasitizing the gills, fins, nasal fossae, tissues and urinary bladder of fishes.
All Ergasilus species known in Brazil are cited as parasitizing only the gills of their hosts. Thirteen
Raphiodon vulpinus (Characiformes: Cynodontidae) from Brazilian Amazon floodplain lakes were
collected and analyzed. The copepod parasite Ergasilus sp. was found in the gills and nasal fossae of this
fish. This is the first record in Brazil of an Ergasilus species parasitizing the gills and nasal fossae of the
same host.
Neotropical Helminthology
525
Neotropical Helminthology, 2017, 11(2), jul-dic: 525-529
RESUMEN
Palabras Clave: Copepoda – lagos inundables – parásito – Raphiodon vulpinus
Especies de Ergasilídeos son encontradas parasitando la branquias, aletas, fosas nasales, tejidos y vejiga
urinaria de peces. Todas las especies de Ergasilus conocidas en Brasil son citadas parasitando sólo las
branquias de sus hospederos. Trece Raphiodon vulpinus (Characiformes: Cynodontidae) provenientes de
lagos inundables de la Amazonía brasileña fueron colectados y analizados. El copépodo Ergasilus sp. fue
encontrado parasitando las branquias y fosas nasales de este pez. Este es el primer registro en Brasil de una
especie de Ergasilus parasitando las branquias y fosas nasales de un mismo hospedero.
INTRODUCTION
526
All known ergasilid species associated with fishes
from Brazil were registered parasitizing or the gills
or the nasal fossae of their host (Luque & Tavares,
2007). This study records for the first time an
Ergasilus species infecting the nasal fossae and
gills of the same host.
Thirteen specimens of R. vulpinus were collected
and examined. Fish were captured in six floodplain
lakes of the Brazilian Amazon between March and
December 2013. The sampled lakes were: Baixio
(03°1 7 ' 2 7,2''S, 60°04 ' 2 9 ,6''W); Preto
(0 3°21'17 ,1''S, 60 °37'28, 6''O); An aná
(03°53'54,8''S, 61°40'18,4''W); São Tomé (03°49'
39,0"S, 61°25' 24,6" W); Araçá (03°45' 04,3" S,
62°21' 25,9"W) and Mara (03°50'32,8''S,
62°34'32,4''W), all lakes located between the cities
of Manaus and Coari in the State of Amazonas.
Copepod parasites were removed from the gill
filaments and nasal fossae of the fish with
dissecting needles and fixed in 70% ethanol. For
taxonomic identification the parasites were
transported to the Fish Parasitology Laboratory of
the National Institute of Amazon Research (INPA),
Manaus, Brazil. Voucher specimens were
deposited in the invertebrate collection of the
National Institute of Amazon Research (INPA),
Manaus, Brazil. Voucher: INPA 2295.
The specimens were stained in 70% ethanol with
small amounts of eosin and orange-G, dehydrated
in pure phenol, cleared in methyl salicylate and
mounted on microscope slides in Canada balsam
(Thatcher, 2006). Drawings were prepared with the
help of a light optical microscope with phase
contrast using a camera lucida.
The prevalence of infection was calculated
according to Bush et al. (1997): prevalence (P) is
the number of infected fish with one or more
individuals of a particular parasite species (or
taxonomic group) divided by the number of hosts
examined (expressed as a percentage).
Copepods are common components in all types of
fish assemblages, being present in all environments
and ecosystems (Boxshall & Halsey, 2004). They
are considered the largest and most diverse group
of crustaceans and the most abundant among
groups of multicellular organisms (Huys &
Boxshall, 1991).
The Ergasilidae von Nordmann, 1832 is one of the
biggest families in the order Cyclopoida
Burmeister, 1835, with most species found on
freshwater fishes. Only adult females of ergasilids
are parasitic on gills, fins, inside the nasal fossae,
embedded in host tissues or in the urinary bladder
of actinopterygian fishes (Boxshall & Halsey,
2004).
The knowledge of the Ergasilidae fauna in the
Americas is irregular, being the species from North
America and Brazil in South America the ones with
the best knowledge (Suárez-Morales et al., 2008).
In Brazil 56 Ergasilidae species are known, being
13 genera and 45 species registered in the Amazon:
Ac us ic ol a (7); A m p l e x i b r a n c h i u s (1);
Brasergasilus (5); Ergasilus (16); Gamidactylus
(3); Gamispatulus (1); Gamispinus (1);
M i r a c e t y m a ( 3 ) ; P i n d a p i x a r a ( 1 ) ;
Prehendorastrus (2); Rhinergasilus (1);
Therodamas (2) and Vaigamus (2) (Luque &
Tavares, 2007).
Rhaphiodon vulpinus Spix & Agassiz, 1829 is
popularly known as 'dourado-facão'. This species
is widely distributed in South America, occurring
in the basins of the Rivers Orinoco, Amazon,
Paraná-Paraguay, Uruguay (Toledo-Piza, 2000)
and the middle and upper Tocantins River
(Neuberger et al., 2007). It is a large, piscivorous
species with significance for sport fishing and
aquaculture (Graça & Pavanelli, 2007).
There are only three crustacean ectoparasites
known from R.vulpinus: Miracetyma kawa Malta,
1993 from Rondônia State, Brazil (Malta, 1993);
Argulus multicolor Stekhoven, 1937 and Dolops
carvalhoi Lemos de Castro, 1949 from Lago
Junuacá, Amazonas, Brazil (Malta, 1984).
MATERIAL AND METHODS
Neotropical Helminthology, 2017, 11(2), jul-dic Murrieta Morey et al.
527
Neotropical Helminthology, 2017, 11(2), jul-dic Ergasilus sp. parasite of gills and nostrils
RESULTS Gamidactylus Thatcher & Boeger, 1984,
Gamispatulus Thatcher & Boeger, 1984;
Gamispinus Thatcher & Boeger, 1984; and
Rhinergasilus Boeger & Thatcher, 1988 are cited
parasitizing the nasal fossae of their hosts
(Thatcher & Boeger, 1983; 1984a, b, c; Boeger &
Thatcher, 1988).
In Amazon floodplain lakes, the ergasilids
Gamidactylus jaraquensis Thatcher & Boeger,
1984 Rhinergasilus piranhus Boeger & Thatcher,
1988; were registered infecting the nasal fossae of
Colossoma macropomum (Cuvier, 1818) and
Serrasalmus altispinis Merckx, Jégu & Santos,
2000 (Morey & Malta, 2016a, b), and Therodamas
elongates Thatcher, 1986 was reported in the nasal
fossae of Astronotus crassipinis (Heckel, 1840)
(Morey et al., 2016).
Some Ergasilus species were found in the nasal
fossae of different fish species: Ergasilus
The parasite identified was Ergasilus sp. (Figure
1). Morphological characters identified in this
parasite assume that this copepod may be a new
species.
Four-hundred seventy-five (475) specimens were
registered parasitizing the gills (456 individuals
collected in Lake Baixio, 17 in Lake Preto and 02 in
Lake Ananá) with a prevalence of 69% and 12 in
the nasal fossae of R. vulpinus (all in Lake Baixio)
with a prevalence of 15%.
In Brazilian freshwater fishes, ergasilid species
from Brasergasilus Thatcher & Boeger, 1983:
DISCUSSION
Figure 1. Ergasilus sp. from Raphiodon vulpinus Spix & Agassiz, 1829. A. whole specimen; B. abdomen and caudal rami, ventral
view. C. Leg V. Scales are given in micrometers (µm).
528
Neotropical Helminthology, 2017, 11(2), jul-dic Murrieta Morey et al.
myctarothes Wilson, 1913 from Sphyrna zigaena
(Linnaeus, 1758) in Jamaica (Wilson 1913), E.
megaceros Wilson, 1916 from Ictalurus anguilla
(Leseur, 1819) in North America (Wilson 1916), E.
rhinus Burris & Miller, 1972 from Centrarchus
macropterus (Lacepède, 1801) Lepomis gibbosus
(Linnaeus, 1758) and L. auritus (Linnaeus, 1758)
(Burris & Miller, 1972).
For Ergasilus, 26 valid species plus 10 unidentified
species have been reported infecting the gills of
Brazilian fishes (Luque & Tavares, 2007) without
any register of occurrence in the nasal fossae. This
is the first report of an Ergasilus species
parasitizing the gills and the nasal fossae of the
same host in the Neotropical region.
Ergasilus sp. is very similar with Ergasilus
xinguensis Taborda, Paschoal & Luque, 2016 by
having the same ornamentations in the antenna, all
endopods 3-segmented and the leg V constitute of a
single segment, well developed. Ergasilus
xinguensis was described from the gills of
Geophagus argyrostictus (Kullander, 1991) (type
host) and G. altifrons (Heckel, 1840) (Taborda et
al., 2016).
The differences found between these two species
are: the type host, site of infection, shape of the
body and some ornamentations in different parts of
the body. A comparative study between these two
species is necessary in order to confirm or not if this
copepod is in fact E. xinguensis or a new species of
Ergasilus. Additionally, a detailed description of
this parasite is being preparing for a future
publication.
We are indebted to the Fish Parasitology
Laboratory team at INPA for the technical
assistance they provided throughout this study.
ACKNOWLEDGEMENTS
Boeger, WA & Thatcher, V. 1988. Rhinergasilus
piranhus gen. et sp. nov. (Copepoda,
BIBLIOGRAPHIC REFERENCES
Poecilostomatoida, Ergasilidae) from the
Nasal Cavities of Piranha Caju,
Serrasalmus nattereri, in the Central
A m a z o n . P r o c e e d i n g s o f t h e
Helminthological Society of Washington,
vol. 55, pp. 87-90.
Boxshall, GA & Halsey, SH. 2004. An introduction
nd
to copepod diversity. 2 ed. Ray Society,
London. 966 pp.
Burris, KW & Miller, CG. 1972. Ergasilus rhinos
sp. n. (Copepoda: Cyclopoida) from the
nasal fossae of three centrarchid fishes of
North Carolina. Journal of Parasitology, vol.
58, pp. 600-604.
Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.
1997. Parasitology meets ecology on its own
terms: Margolis et al. revisited. The Journal
of parasitology, vol. 83, pp. 575-583.
Dogiel, VA. 1961. Ecology of the parasites of
freshwater fishes. Parasitology of fishes, In
VA. Dogiel, GK. Petrushevski & Polyanski,
YI. (eds.). Parasitology of Fishes. Oliver &
Boyd, Edinburg, pp. 1-47.
Graça, WJ & Pavanelli, CG. 2007. Peixes da
planície de Inundação do Alto Rio Paraná e
áreas adjacentes. Eduem, Maringá, 241 pp.
Huys, R & Boxshall, G. 1991. Copepod evolution.
The Ray Society, London. 468 pp.
Luque, JL & Tavares, LE. 2007. Checklist of
Copepoda associated with fishes from
Brazil. Zootaxa, vol. 1579, pp. 1-39.
Malta, JC. 1983. Miracetyma kawa sp. nov.
( C o p e p o d a , P o e c i l o s t o m a t o i d a ,
Ergasilidae) from Freshwater Fishes of the
Brazilian Amazon. Acta Amazonica, vol. 23,
pp. 251-259.
Malta, JC. 1984. Os peixes de um lago de várzea da
Amazônia Central (Lago Janauacá, Rio
Solimões) e suas relações com os crustáceos
ectoparasitas (Branchiura: Argulidae).
Acta Amazonica 14, pp. 355-372., vol.
Morey, GA & Malta, JC. 2016a. Metazoários
parasitas das narinas do tambaqui
Colossoma macropomum (Cuvier, 1818)
(Characiformes: Characidae) coletadas em
lagos de várzea da Amazônia central,
Brasil. Folia Amazónica 25, pp. 71-76., vol.
Morey, GA & Malta, JC. 2016b. As espécies de
Copepoda (Crustacea: Ergasilidae)
parasitas dos filamentos branquiais e
narinas de Serrasalmus altispinis (Merckx,
J é g u e S a n t o s , 2 0 0 0 )
529
Neotropical Helminthology, 2017, 11(2), jul-dic Ergasilus sp. parasite of gills and nostrils
(Characiformes–Serrasalmidae) em lagos
de várzea do brasil. Folia Amazónica, vol.
25, pp. 55-60.
Morey, GA, Moreira, AC, Morais, AM, Atroch, FB,
Santana, HP, Brandão, NR, Dumbo, JC,
Vital, JF & Malta, JC. 2016. Copepods
(Crustacea: Ergasilidae) fish parasites of
floodplain Lakes of Central Amazon, Brazil.
Neotropical Helminthology, vol. 10, pp. 281
294.
Suárez-Morales, E & Santana, AM. 2008. A new
sp e ci e s o f E rga sil us ( Co p ep o da :
Cyclopoida: Ergasilidae) from coastal
fishes of the Mexican Pacific. Folia
parasitológica, vol. 55, pp. 224-230.
Taborda, NL, Paschoal, F & Luque, JL. 2016. A
new species of Ergasilus (Copepoda:
Ergasilidae) from Geophagus altifrons and
G. argyrostictus (Perciformes: Cichlidae) in
the Brazilian Amazon. Acta Parasitologica,
vol. 61, pp. 549-555.
Thatcher, VE. 2006. Amazon fish parasites.
Pensoft Publishers, 2nd ed. Sofia-Mosoow,
508 pp.
Thatcher, VE & Boeger, WA. 1983. The parasitic
crustaceans of fishes from the Brazilian
A m a z o n . 5 . B r a s e rg a s i l u s g e n .
nov.(copepoda: cyclopidea), a" three-
legged" ergasilid, with two new species and
the proposal of Abergasilinae subfam. nov.
Acta Amazonica, vol. 13, pp. 195-214.
Thatcher, VE & Boeger, WA. 1984a. The parasitic
crustaceans of fishes from the Brazilian
Amazon. 13. Gamidactylus jaraquensis gen.
et sp. nov. (Copepoda, Poecilostomatoida,
Vaigamidae) from the nasal fossae of
Semaprochilodus insignis (schomburgk).
Amazoniana limnologia et Oecologia
Regionalis Systemae Fluminis Amazonas
vol. 8, pp. 421-426.
Thatcher, VE & Boeger, WA. 1984b. The parasitic
Crustaceans of fishes from the Brazilian
Amazon, 15, Gamispatulus schizodontis
g e n . e t s p . n o v . ( C o p e p o d a :
Poecilostomatoida: Vaigamidae) from the
nasal fossae of Schizodon fasciatus.
Amazoniana, vol. 9, pp. 119-126.
Thatcher, VE & Boeger, WA. 1984c. The parasitic
crustaceans of fishes from the Brazilian
Amazon. 14. Gamispinus diabolicus gen. et
sp. nov. (Copepoda, Poecilostomatoida,
Vaigamidae) from the nasal fossae of
Ageneiosus brevifilis Valenciennes.
Amazoniana limnologia et Oecologia
Regionalis Systemae Fluminis Amazonas,
vol. 8, pp. 505-510.
Toledo-Piza, M. 2000. The Neotropical fish
subfamily Cynodontinae (Teleostei:
O s t ar io p h y si : Ch a r a ci fo r m e s) : a
phylogenetic study and a revision of
Cynodon and Rhaphiodon. American
Museum Novitates, New York, 88 pp.
Received October 18, 2017.
Accepted October 31, 2017.