ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2018, 12(1), ene-jun:21-26.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

MONOGENOIDEANS PARASITIZING RHAPHIODON VULPINUS SPIX & AGASSIZ, 1829

(CHARACIFORMES: CYNODONTIDAE) FROM LAKES BAIXIO AND CATALÃO,

AMAZONAS, BRAZIL

MONOGENÓIDEOS PARASITANDO RHAPHIODON VULPINUS (CHARACIFORMES:

CYNODONTIDAE) PROVENIENTES DE LOS LAGOS BAIXIO Y CATALÃO, AMAZONAS, BRASIL

1 Laboratório de Ecologia Molecular e Parasitologia Evolutiva (LEMPE), Universidade Federal do Paraná (UFPR), Rua

Evaristo F. F. da Costa 418, Jardim das Américas, Curitiba – PR, 80050-540. 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. jcmalta@inpa.gov.br

1 2

Germán Augusto Murrieta Morey & José Celso de Oliveira Malta

ABSTRACT

Keywords: floodplain lakes – gills – nostrils – Notozothecium lamotheargumedoi – Rhinoxenus piranhus

Rhaphiodon vulpinus Spix & Agassiz, 1829 is a neotropical fish species that inhabits lakes and rivers

throughout the Orinoco, Amazonas and Prata basins, and rivers of the Atlantic slopes of the Guianas. Up to

now in the Neotropical region, only one species of Monogenoidea is known from this fish. The present

study aims to identify the monogenoideans that parasitize R. vulpinus collected in two floodplain lakes.

Twelve specimens of R. vulpinus were captured and examined from Lake Baixio and 32 specimens from

Lake Catalão, both located in the township of Iranduba, Amazonas, Brazil. Two species of Monogenoidea

were identified: Notozothecium lamotheargumedoi Cohen & Kohn, 2008 infecting the gills and

Rhinoxenus piranhus Kritsky, Boeger & Thatcher, 1988 infecting the nostrils. Notozothecium

lamotheargumedoi is reported for the second time in R. vulpinus, while R. piranhus is cited for the first

time in a cynodontid species, increasing the number of known hosts for this parasite.

Neotropical Helminthology

INTRODUCTION

RESUMEN

Palabras clave: branquias – fosas nasales – lagos – Notozothecium lamotheargumedoi – Rhinoxenus piranhus

Rhaphiodon vulpinus Spix & Agassiz, 1829, es una especie de pez neotropical que habita lagos y ríos de

las vacías del Orinoco, Amazonas y Prata, y en ríos de los declives atlánticos de las Guayanas. Hasta ahora

en la región Neotropical, sólo una espécie de Monogenoidea es conocida para esta especie de pez. El

presente estudio pretende identificar las especies de monogenóideos que parasitan R. vulpinus colectados

en dos lagos inundables. Doce especímenes de R. vulpinus provenientes del lago Baixio y 32 especímenes

del lago Catalão, localizados en el município de Iranduba, Amazonas, Brasil, fueron capturados y

examinados. Dos especies de monogenóideos fueron identificadas: Notozothecium lamotheargumedoi

Cohen & Kohn, 2008 infectando las branquias y Rhinoxenus piranhus Kritsky, Boeger & Thatcher, 1988

en las fosas nasales Notozothecium lamotheargumedoi es citado por segunda vez en R. vulpinus, mientras

que, R. piranhus es citada por primera vez en una especie de cynodontídeo, aumentando el número de

hospederos conocidos para este parásito

For cynodontines, Domingues & Boeger (2005)

reported undetermined species of Rhinoxenus from

Hydrolicus scomberoides (Cuvier, 1819) and

posteriorly, Cohen & Kohn (2008) described

Notozothecium lamoarthogumedoi from the gills

of R. vulpinus collected in different localities of the

Paraná River, State of Paraná, Brazil, being the

only monogenoidean known for cynodontids. The

last report from a monogenoidean parasitizing a

cynodontid was made by Kohn et al. (2011) who

reported an undetermined species from R. vulpinus

collected in the reservoir of the Hydroelectric

Power Station of Itaipu, Paraná, Brazil.

During an investigation in two Amazon floodplain

lakes, two species of Monogenoidea were recorded

from the gills and nostrils of the cynodontid

freshwater fish R. vulpinus.

Between March and December 2013, 12 R.

vulpinus (Fig. 1) were captured in Lake Baixio

0 0

(03 17'27, 2''S/ 60 04'29,6''W) in the township of

Iranduba, and between March and July 2016, 32 R.

vulpinus were captured in Lake Catalão (3 10'04''S/

59 54'45''W), also in Iranduba, Amazonas, Brazil.

Fish were caught using 100 mm between adjacent

nodes-meshed, 20 m long x 2 m high gillnets.

Cynodontidae comprises 13 species grouped into

two subfamilies: Cynodontinae with the genera

Cynodon Agassiz, 1829; Hydrolycus Cuvier, 1819;

Rhaphiodon Spix & Agassiz, 1829 and Roestinae

with the genera Gilbertolus (Steindachner, 1878),

and Roestes (Kner, 1858) (Lucena & Menezes,

1998). Cynodontines inhabit rivers, lakes, and

flooded forests in all water types, throughout the

Orinoco, Amazonas and Prata basins, and in rivers

of the Atlantic slopes of the Guianas (Toledo-Piza,

2000).

Rhaphiodon vulpinus Spix & Agassiz, 1829 is a

neotropical fish species identified by the oblique

mouth, large canine teeth and relatively long

pectoral fins (Lucena & Menezes, 1998). In lakes,

adults are caught in open areas and in the flooded

forest. Young specimens are caught in the aquatic

vegetation (Saint-Paul et al. 2000). It is a pelagic

and migratory fish, with diurnal habit, piscivorous,

hunting in shoals and predates its prey swallowing

it whole (Pouilly et al., 2004).

The class Monogenoidea is very diverse in number

of species, morphology and ecology (Poulin &

Valtonen 2002). Monogenoideans are found

parasitizing the skin, outer and inner organs of

several aquatic vertebrates, and they are well

known by their high host and infestation site's

specificity (Poulin, 1992).

MATERIAL AND METHODS

Murrieta Morey et al.

Neotropical Helminthology, 2018, 12(1), ene-jun

RESULTS

Posteriorly, fishes were quickly immersed in 75 mg

-1

clove oil·L solution and euthanized following the

recommendations of the Ethics and Animal

Welfare Committee (CONCEA, 2013). In the field,

fishes were measured and weighed and posteriorly

gills and nostrils were removed and preserved in

formalin 5% for posterior analyses at the

laboratory of Fish Parasitology (LPP) in the

National Institute of Amazonian Research (INPA).

For morphological studies, the parasites were

mounted in Grey and Wess medium (Amato et al.,

1991). Taxonomical identification was according

to Cohen & Kohn (2008) and Kritsky et al. (1988).

Voucher specimens were deposited in the

Crustacean Collection of the National Institute of

Amazon Research (INPA), Manaus, AM, Brazil

(INPA – 643 and 644). The ecological terms in

parasitology follow Bush et al. (1997).

Notozothecium lamotheargumedoi (Fig. 2) was

found parasitizing the gills of R. vulpinus collected

in both lakes, while Rhinoxenus piranhus (Fig. 3)

was found in the nostrils from specimens collected

only in the Lake Baixio. The highest parasitic

levels were registered for N. lamotheargumedoi

(Table 1).

Figure 1. Lateral view of Raphiodon vulpinus Spix & Agassiz, 1829 collected in Amazon oodplain lakes

Figure 2. A. Total body of Notozothecium lamotheargumedoi Cohen & Kohn, 2008 collected from Rhaphiodon vulpinus Spix &

Agassiz, 1829. cc = copulatory complex, B. male copulatory complex. ci = cirrus, ap = accessory piece. C. Haptor. vb = ventral

bar.

Monogenoideans parasitizing Rhaphiodon

Neotropical Helminthology, 2018, 12(1), ene-jun

Notozothecium species were reported only for

Characiformes (Characidae and Serrasalmidae)

(Cohen et al., 2013). Notozothecium

lamotheargumedoi seems to be very specific and

was only cited for R. vulpinus (Cohen & Kohn,

2008) being the only species of Notozothecium

reported for a species of Cynodontidae. In the

present study, N. lamotheargumedoi is reported for

the second time in R. vulpinus, expanding its

geographic distribution to the state of Amazonas.

Figure 3. A. total body of Rhinoxenus piranhus Kritsky, Boeger & Thatcher, 1988 collected from Rhaphiodon vulpinus Spix &

Agassiz, 1829. B. anterior part. cc = copulatory complex, v = vagine, C. Haptor. da = dorsal anchor, va = ventral anchor, vb =

ventral bar.

Table 1. Parasitic indexes of the Monogenean parasite species in Rhaphiodon vulpinus Spix & Agassiz, 1829

collected in Amazon floodplain lakes. N = number of examined fish, Ni = number of infected fish, P% = prevalence, I

= intensity of infection, mI = mean intensity of infection, mA = mean abundance.

Species

Lake N Ni P% I mI mA

Notozothecium lamotheargumedoi

Baixio 12 6 50 1090 181.66

90.83

Catalão 32 32 100 1372 42.88 42.88

Rhinoxenus piranhus

Baixio 12 3 25 10 3.33 0.83

DISCUSSION If a parasitic species infects a host belonging to a

small family, the probability of a close coevolution

between the parasite and the host species will be

greater than if the host belongs to a larger family in

which the colonization of a new host will be more

frequent (Poulin, 1992). This is probably the case

of N. lamotheargumedoi which parasitizes R.

vulpinus, a fish from a small family in which the

coevolutionary processes may be stronger,

resulting in high parasite-host specificity.

The chemical composition of fish skin is well

known to be species-specific. Initial contact

between the adhesive areas of oncomiracidium

Murrieta Morey et al.

Neotropical Helminthology, 2018, 12(1), ene-jun

Amato, JFR, Boeger, WA & Amato, SB. 1991.

Protocolos para laboratório coleta e

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Imprensa Universitária, Universidade

Federal do Rio de Janeiro, Rio de Janeiro,

Brasil. 81 pp.

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1997. Parasitology meets ecology on its

own terms: Margolis et al. revisited. The

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583.

Cohen, SC, Kohn, A. 2008. Una especie nueva del

género Notozothecium (Monogenea,

Dactylogyridae), parásita de Rhaphiodon

vulpinus (Cynodontidae, Characiformes)

del río Paraná, estado de Paraná, Brasil.

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Cohen, S, Justo, M & Kohn, A. 2013. South

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Eiras, JC, Takemoto, RM, Pavanelli, GC &

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Iannacone, JA & Luque, JL. 1993. New records of

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larvae and host epidermis may contribute to the

interaction of the sensory organs of the parasite

with the specific chemicals of the host epidermis

and the recognition between those components and

the adherents secreted by monogeneans

(Whittington et al., 2000). The occurrence of N.

lamotheargumedoi only in R. vulpinus is a clear

example of host-specificity, where apparently

exists a specialized communication between both

organisms, which allows this parasite species

recognize and parasitize this fish.

Rhinoxenus spp. were recorded parasitizing the

nostrils of some Anostomidae, Bryconidae,

Prochilodontidae and Triportheidae species (Eiras

et al., 2010; Moreira et al., 2017). R. piranhus was

registered only on Serrasalmidae species in three

different countries. In Brazil, it was cited on

Pygocentrus nattereri Kner, 1858 and Serrasalmus

altuvei Ramírez, 1965 (Kritsky et al., 1988; Vital et

al., 2011; Morais et al., 2012), in French Guiana on

P. nattereri and S. spilopleura Kner, 1858

(Domingues & Boeger, 2005) and in Peru on P.

nattereri (Iannacone & Luque, 1993; Luque et al.,

2016). In the present study R. piranhus is recorded

for the first time in the nostrils of a Cynodontidae

especies, increasing the number of known hosts for

this parasite.

The high values in the parasitic indexes of N.

lamotheargumedoi indicate its efficiency on the

transmission of new individuals and the

colonization of the gills of R. vulpinus. Lentic

environments such as the Lake Baixio and Catalão,

facilitate the life cycle of this parasites, influencing

positively in the abundance of specimens that

parasitize the gills of this fish. In contrast, R.

piranhus seems to be less efficient. This could be,

because the nostrils are smaller than the gills, so the

space of colonization is reduced.

The authors thank the support of Laboratorio de

Parasitologia de Peixes (LPP) of the Instituto

Nacional de Pesquisas da Amazonia - INPA.

GAMM received a scholarship from the

Coordenação de Aperfeiçoamento de Pessoal de

Nível Superior – CAPES (Brazil).

ACKNOWLEDGEMENTS

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Accepted February 5, 2018.

Murrieta Morey et al.

Neotropical Helminthology, 2018, 12(1), ene-jun