Neotrop. Helminthol., 6(1), 2012

2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

Abstract

A study on the nematode parasites of nine species of freshwater fishes from Peixe River São Paulo,

State, Brazil. was conducted. Fish were collected between February 2010 and March 2011 and the

following species were found: Procamallanus (Spirocamallanus) inopinatus and Contracaecum sp.

(larvae) in Astyanax altiparanae; Contracaecum sp. (larvae), Dioctophyma renale (larvae),

Philometroides caudata, P. (Spirocamallanus) inopinatus, P. (Spirocamallanus) neocaballeroi

(larvae) and P. (Spirocamallanus) saofranciscensis in Acestrorhynchus lacustris; Contracaecum sp.

(larvae), Guyanema sp., Hysterothylacium sp. (larvae) and Icthyouris sp. in Cyphocharax modestus;

Contracaecum sp. (larvae), Cosmoxynemoides aguirrei and Pharyngodonidae gen. sp. in C. nagelii;

Dioctophyma renale (larvae), Hysterothylacium sp. (larvae) and Rhabdochona sp. in Gymnotus

sylvius; Capillariidae gen. sp. in Hoplosternum littorale; Cosmoxynema vianai, Guyanema sp.,

Ichthyouris sp. and Travnema travnema in Steindachnerina insculpta; Contracaecum sp. (larvae),

Procamallanus (Spirocamallanus) rebecae (larvae) in Triportheus angulatus and Rhabdochona

acuminata in Triportheus nematurus. This is first study of nematode parasites from the Peixe River,

therefore all the species found are new geographical records and 19 are new host records.

Key words: Acestrorhynchidae – Biodiversity – Callichthyidae – Characidae – Curimatidae - Gymnotidae -

Helminthes - Parasites.

NEW HOSTS AND DISTRIBUTION RECORDS FOR NEMATODE PARASITES OF

FRESHWATER FISHES FROM SÃO PAULO STATE, BRAZIL

NUEVO HOSPEDADORES Y REGISTROS DE DESTRIBUCIÓN PARA

NEMATODOS PARÁSITOS DE PECES DE ÁGUA DULCE DEL ESTADO DE

SÃO PAULO, BRASIL

Vanessa Doro Abdallah*, Rodney Kozlowiski de Azevedo, Edmir Daniel Carvalho & Reinaldo José da Silva

UNESP- Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociências,

Departamento de Parasitologia, Botucatu, São Paulo, Brazil.

*E-mail: vanessaabdallah@ig.com

Suggested citation: Abdallah, VD, Azevedo, RK, Carvalho, ED & Silva, RJ. 2012. New hosts and distribution records for

nematode parasites of freshwater fishes from São Paulo State, Brazil. Neotropical Helminthology, vol. 6, nº1, pp. 43 - 57.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

Resumen

Palabras clave: helmintos - parásitos.

Acestrorhynchidae – Biodiversidad – Callichthyidae – Characidae – Curimatidae - Gymnotidae -

Se llevó a cabo un estudio de los nematodos parásitos de nueve especies de peces de agua dulce del Río

do Peixe, Estado de São Paulo, Brasil. Los peces fueron colectados entre febrero de 2010 y marzo de

2011 y las especies encontradas fueron: Procamallanus (Spirocamallanus) inopinatus y

Contracaecum sp. (larva) en Astyanax altiparanae; Contracaecum sp. (larva), Dioctophyma renale

(larva), Philometroides caudata, P. (Spirocamallanus) inopinatus, P. (Spirocamallanus)

neocaballeroi (larva) y P. (Spirocamallanus) saofranciscensis en Acestrorhynchus lacustris;

Contracaecum sp. (larva), Guyanema sp., Hysterothylacium sp. (larva) y Icthyouris sp. en

Cyphocharax modestus; Contracaecum sp. (larva), Cosmoxynemoides aguirrei y Pharyngodonidae.

gen. sp. en C. nagelii; Dioctophyma renale (larva), Hysterothylacium sp. (larva) y Rhabdochona sp. en

Gymnotus sylvius; Capillariidae gen. sp. en Hoplosternum littorale; Cosmoxynema vianai, Guyanema

sp., Ichthyouris sp. y Travnema travnema en Steindachnerina insculpta; Contracaecum sp. (larva),

Procamallanus (Spirocamallanus) rebecae (larva) en Triportheus angulatus y Rhabdochona

acuminata en Triportheus nematurus. Este es el primer estudio de nemátodos parásitos de Río do

Peixe, por lo tanto todas las especies son nuevos registros geográficos y 19 son nuevos registros de

hospedadores.

Abdallah et al.

Nematode parasites of freshwater fishes of Brazil

Parasitic nematodes constitute one of the earliest

known groups of helminthes in fishes. They infect

freshwater, marine and brackish water fish species

and sometimes cause substantial damage to the

host. Although parasitic nematodes can infect

almost all fish organs, the majority of the currently

known species has been described from the

intestine. Most nematodes infect fish as adults, but

a large proportion of them occur as larval stages.

These are usually parasites of piscivorous birds,

mammals or reptiles, or less frequently of

predatory fishes (Molnár et al., 2006). These

helminthes cause considerable economic loss in

the fishery industries (Thatcher, 2006). Since

many nematode larvae are large enough to be seen

by the naked eye, their presence can make fish

unmarketable (Thatcher, 2006). The damage

caused to fish by nematodes varies greatly

INTRODUCTION depending on the species, organ infected and

intensity of infection (Thatcher, 2006). Among the

nematodes parasitizing fishes, anisakid species

causing human infections are well documented

(Molnár et al., 2006).

Currently, the biodiversity of freshwater

ecosystems of Latin America is threatened, mainly

by environmental problems resulting from the

degradation of the ecosystems. In this context,

parasite biodiversity can be very important

because parasitism plays a key role in ecosystems,

regulating the abundance or density of host

populations, stabilize food webs and structuring

animal communities. Thus, knowledge of parasite

diversity and its possible decline are crucial for

environmental management and conservation

(Luque & Poulin, 2007). Therefore, biotic

diversity studies are presently conducted with a

sense of urgency and they underscore the need for

baseline biological inventories and surveys. The

faunal survey is critical, because even the most

Neotrop. Helminthol., 6(1), 2012

elementary information is lacking for many groups

in many parts of the Neotropics (Moravec, 1998).

Considering the rapid development of marine,

brackish-water and freshwater aquaculture in

different countries during recent years, the

significance of nematodes as important fish

pathogens is also increasing. However, the present

knowledge of these parasites is very incomplete,

particularly in regard to their biology and ecology,

but also in taxonomy, geographical distribution

and others aspects (Moravec, 1998).

The Peixe River (48º06'38”W, 22º49'53.1”S)

(Fig.1) is a tributary on the left bank of the middle

Tiete River Basin in the region of Barra Bonita,

São Paulo State (SP), Brazil. This river originates

in the municipality of Torre de Pedra (SP) in the

Basaltic Cuesta Botucatu Environmental

Preservation Area and is a drainage basin

corresponding to 584 km running north-south

(Caramaschi, 1986).

To date, there are no studies on nematodes

parasites in the Peixe River. The aim of this is to

report the nematode species associated with fishes

from this river.

Four hundred forty-eight fish specimens

belonging to nine species from Peixe River,

municipality of Anhembi, São Paulo State, Brazil,

were collected between February 2010 and March

2011 in order to study of their nematodes. The

protocol for collection of fishes and nematodes are

in accordance with the protocols recommended by

the ethics committee and authorized by the

IBAMA/ICMBio (license 15549-1).

Fish were collected using nylon monofilament gill

nets with mesh sizes of 3–14 cm from three sites on

the Peixe River. Nets were placed at 5:00 p.m. and

removed at 7:00 a.m. the following day, total

exposure 14 h. Fishes were taken from nets and

each specimen was separated in plastic bags. Some

fish specimens were maintained in coolers until

necropsy that was realized until one hour after the

collection and others were frozen and analyzed

posteriorly. Organs were removed, washed and

sieved in mesh of 75 µm aperture. The nematodes

collected were fixed in alcohol 70 ºGL. For the

identification the specimens were mounted in

lactophenol. The ecological descriptors of

parasitism were calculated according Bush et al.

(1997).

Voucher specimens were deposited in the Coleção

Helmintológica do Instituto de Biociências de

Botucatu (CHIBB), São Paulo State, Brazil.

Seventeen taxa of nematodes (Table 1) were

collected, as follow: Capillariidae gen. sp. (Figure

2 ), Contracaecum sp. (larvae) (Figures 2 ),

A B-D

Cosmoxynema vianai Travassos, 1948 (Figures 2E-

), Cosmoxynemoides aguirrei Travassos, 1948

(Figures 3 ), Dioctophyma renale (Goeze, 1782)

A-B

(larvae) (Figures 3 ), Guyanema sp. (Figures 3

C-D E-

), Hysterothylacium sp. (larvae) (Figures 4 ),

F A-B

Icthyouris sp. (Figures 4 ), Pharyngodonidae gen.

C-D

sp., Philometroides caudata Moravec, Scolz &

Vivas-Rodríguez, 1995 (Figures 4 ),

E-F

Procamallanus (Spirocamallanus) inopinatus

Tr a vas s o s , 1 929 (Fig u r e s 5 ), P.

A - B

(Spirocamallanus) neocaballeroii (Caballero-

Deloya, 1977) (Figures 5 ), P. (Spirocamallanus)

C-D

rebecae (Andrade-Salas, Pineda-López & García-

Magaña, 1994) (Figures 5 ), P. (Spirocamallanus)

E-F

saofranciscensis (Moreira, Oliveira & Costa,

1994) (Figure 6 ), Rhabdochona acuminata

(Molin, 1860) (Figures 6 ), Rhabdochona sp., and

B-D

Travnema travnema Pereira, 1938 (Figures 6 ).

E-F

Five out of 17 species of nematodes were larvae.

The nematode species with lower specificity was

the Contracaecum sp. (larvae), which was reported

in five host species. Acestrorhynchus lacustris

(Lütken, 1875) presented the greatest richness of

nematodes, with six nematode species found. The

main infection site was the intestine, which was

parasitized by all parasite species.

MATERIAL AND METHODS

RESULTS

Abdallah et al.

Nematode parasites of freshwater fishes of Brazil

Table 1. Nematode parasites of fishes from Peixe river, São Paulo State, Brazil. N – number of fish; SI – site of infection; P – prevalence (%); MII – mean intensity of infection; MA –

mean abundance; SD standard deviation; CHIBB – Coleção Helmintológica do Instituto de Biociências de Botucatu; *new host record.

Contracaecum sp.

(larvae)

CHIBB 6808

Intestine

13.3

0.13

Astyanax altiparanae

Garutti & Britski, 2000

Procamallanus (Spirocamallanus) inopinatus

CHIBB 6809

Stomach

and

intestine

73.3

1.45 ± 0.07

1.06 ± 0.05

Contracaecum sp.(larvae)

CHIBB 6810

Stomach, liver

and

intestine

2.40 ± 0.33

0.60 ± 0.08

Dioctophyma

renale

(larvae)*

CHIBB 6811

Intestine

0.05

Philometroides

caudata*

CHIBB 6812

Intestine

0.10

Procamallanus (Spirocamallanus) inopinatus*

CHIBB 6813

Intestine

0.10

Procamallanus ( Spirocamallanus) neocaballeroii

(larvae)*

CHIBB 6814

Intestine

0.10

Acestrorhynchus lacustris

(Lütken, 1875)

Procamallanus

(Spirocamallanus) saofranciscensis

CHIBB 6815

Intestine

0.10

Contracaecum sp.

(larvae)*

CHIBB 6816

Liver

0.10

Guyanema sp.*

CHIBB 6817

Intestine

0.20

Hysterothylacium sp. (larvae)*

CHIBB 6818

Intestine

0.10

Cyphocharax modestus

(Fernández-Yépez, 1948)

Icthyouris sp.*

CHIBB 6819

Intestine

1.50 ± 0.35

0.30 ± 0.07

Contracaecum sp.

(larvae)*

CHIBB 6820

Liver and

intestine

0.20

Cyphocharax nagelii

(Steindachner, 1881)

Cosmoxynemoides aguirrei*

CHIBB 6821

Intestine

6,17 ± 7,86

1,43 ± 4,41

Pharyngodonidae gen. sp.*

CHIBB 6822

1 0.10

Host

Parasite

MII ± SD

MA ± SD

Neotrop. Helminthol., 6(1), 2012

Dioctophyma renale (larvae)*

CHIBB 6823 Intestine 20 1.50 ± 0.35 0.30 ± 0.07

Hysterothylacium sp. (larvae)*

CHIBB 6824 Intestine 10 1 0.10

Gymnotus silvyus

Albert & Fernandes-Matioli,

1999

Rhabdochona sp.*

CHIBB 6825 Stomach and

intestine 20 6 1.20

Hoplosternum littorale

(Hancock, 1828)

60 Capillariidae gen. sp.

CHIBB 6826 Stomach,

intestine and

liver

19.3 2.00 ± 0.21 0.40 ± 0.04

Cosmoxynema vianai

CHIBB 6827 Intestine 6.6 1.00 ± 0.19 1.00 ± 0.03

Guyanema sp.*

CHIBB 6828 Intestine 6.6 0.40 ± 0.20 0.13 ± 0.01

Ichthyouris sp.*

CHIBB 6829 Intestine 6.6 1 0.06

Steindachnerina insculpta

(Fernández-Yépez, 1948)

Travnema travnema

CHIBB 6830 Intestine 13.3 2.75 ± 0.13 0.35 ± 0.01

Contracaecum sp. (larvae)*

CHIBB 6831 Intestine 17 1.00 ± 0.19 1.00 ± 0.03 Triportheus angulatus (Spix

& Agassiz, 1829) 17

Procamallanus (Spirocamallanus) rebecae (larvae)*

CHIBB 6832 Intestine 20 1 0.20

Triportheus nematurus

(Kner, 1858) 2 Rhabdochona acuminata*

CHIBB 6833 Intestine 50 6.00 ± 4.24 3.00 ± 2.12

(Continued Table 1)

Host

Parasite

MII ± SD

MA ± SD

Abdallah et al.

Nematode parasites of freshwater fishes of Brazil

Table 2. Parasitological records in host studied in others Hidrographic Basins.

Hosts Nematodes Localities References

Contracaecum sp.

Procamallanus (Spirocamallanus) caballeroi

Procamallanus (Spirocamallanus) inopinatus

Astyanax altiparanae

Garutti & Britski, 2000

Spiroxys sp.

Paraná River

Pond in Aguai, São Paulo

State

Takemoto et al. (2009)

Saraiva et al. (2006)

Contracaecum sp.

Contracaecum Type 1

Contracaecum Type 2

Eustrongylides sp.

Heterotyphlum sp.

Philometridae

Procamallanus sp.

Procamallanus (Spirocamallanus) paraensis

Spirocamallanus saofranciscensis

Travassosnema

travassosi paranaensis

Acestrorhynchus lacustris

(Lütken, 1875)

Travassosnema travassosi travassosi

Amazon Basin

Mogi Guaçu River

Paraná River

São Francisco River

Tibagi River

Buhrnheim (1976)

Carvalho et al. (2003)

Costa et al. (1991)

Moravec et al. (1993)

Moreira et al. (1994)

Silva-Souza & Saraiva (2002)

Takemoto et al. (2009)

Thatcher (2006)

Capillariidae gen. sp. Hoplosternum littorale

(Hancock, 1828) Goezia sp. Guandu River Abdallah et al. (2006)

Cosmoxynema vianai Steindachnerina insculpta

(Fernández-Yépez, 1948) Travnema travnema Paraná River Takemoto et al. (2009)

Triportheus angulatus

(Spix & Agassiz, 1829) Procamallanus (Spirocamallanus) inopinatus Laguna de Yarinacocha,

Ucayali-Peru Iannacone et al. (2000)

Neotrop. Helminthol., 6(1), 2012

Figure 1. Map of the study area, showing details of river and their geographic coordinates.

Abdallah et al.

Nematode parasites of freshwater fishes of Brazil.

Figure 2. A. Detail of eggs (arrow) of Capillaridae gen. sp.; B. Cephalic extremity of Contracaecum sp., showing

the excretory pore (arrow); C. Region of ventriculus of Contracaecum sp., showing (C=caecum, O=oesophagus,

V=ventriculus and VA=ventricular appendix); D. Posterior extremity of Contracaecum sp. showing the absence of

mucrons; E. Anterior end of body of Cosmoxynema vianai; F. Tail of Cosmoxynema vianai showing the eggs

(arrow).

50 µm 50 µm

100 µm

200 µm

100 µm

Neotrop. Helminthol., 6(1), 2012

Figure 3. A. Anterior end of body of Cosmoxynemoides aguirei; B Head end of Cosmoxynemoides aguirei; C.

Anterior end of body of Dioctophyma renale showing the junction of oesophagus and intestine (arrow); D. Posterior

end of male larva of Dioctophyma renale showing the genital bursa (arrow); E. Anterior end of body of Guyanema

sp.; F. Gravid specimen of Guyanema sp., showing the uterus with larvae (arrow).

100 µm

50 µm

100 µm

Abdallah et al.

Nematode parasites of freshwater fishes of Brazil.

Figure 4. A. Tail of Hysterothylacium sp. showing the mucrons; B. Cephalic extremity of Hysterothylacium sp.; C.

Cephalic extremity of Icthyouris sp.; D. Tail of Icthyouris sp. showing the lateral alae; E. Cephalic extremity of

Philometroides caudate, showing the ring of slightly elevated cuticle; F. Tail of Philometroides caudata.

100 µm

Neotrop. Helminthol., 6(1), 2012

Figure 5. A. Buccal capsule of Procamallanus (Spirocamallanus) inopinatus; B. Posterior end of male of

Procamallanus (Spirocamallanus) inopinatus, showing the spicules almost equal in length (arrow); C. Buccal

capsule of Procamallanus (Spirocamallanus) neocaballeroi; D. Posterior end of Procamallanus (Spirocamallanus)

neocaballeroi, showing the tip of tail (arrow); E. Buccal capsule of Procamallanus (Spirocamallanus) rebecae; F.

Posterior end of Procamallanus (Spirocamallanus) rebecae, showing the tip of tail (arrow).

µm

Abdallah et al.

Nematode parasites of freshwater fishes of Brazil.

Figure 6. A. Buccal capsule of Procamallanus (Spirocamallanus) saofranciscencis; B. Anterior end of

body of Rhabdochona acuminata; C. Vulva of Rhabdochona acuminate (arrow); D. Posterior end of

male, showing the small and larger spicules of Rhabdochona acuminate (arrow); E. Anterior end of body

of Travnema travnema showing the buccal capsule without teeth (arrow); F. Posterior end of body of

Travnema travnema showing the eggs (arrow).

µm

100

µm

100

µm

Seventen nematode taxa were here reported in

fishes from Peixe River, São Paulo State, Brazil.

All helminthes collected represent new

geographic distribution. Nineteen new host

records are reported. In addition, this is the first

record of nematodes in C. modestus, C. nagelii,

G. silvyus and T. nematurus.

The larva that showed low specificity was

Contracaecum sp. This species belongs to the

family Anisakidae and has great importance in

public health due its high zoonotic potential.

Anisakids are important to humans on a number

of counts, such as economically, politically and

mainly pathologically (Takemoto et al., 2009).

Anisakiasis in humans can occur by eating the

flesh of the fish raw or insufficiently heat-

treated, salted or smoked, containing larvae of

the third or fourth stage, in which case the man

acts as an accidental host and the larvae do not

complete their development. These parasites can

penetrate the human digestive tract and invade

the organs causing a series of attachment

pathological effects (Lymbery & Cheah, 2007).

However, the results presented in this paper

indicate that no problem can be related to this

finding since all anisakid larvae found were

encysted or free in the stomach, intestine and

liver, which are not used for human

consumption.

In relation to nematodes, it is known that fishes

can act as intermediate or definitive host. In

present paper the majority of fishes species

studied were parasitized by adult forms,

indicating that they occupy a final position in the

food web.

We found higher diversity of nematodes in this

study when compared with works performed in

others water systems (Table 2). The comparative

qualitative analysis of nematode fauna between

the fishes of this study in relation to the same

species from other localities revealed similarity

only four nematode species: Contracaecum sp.

and P. (Spirocamallanus) inopinatus in A.

altiparanae; Contracaecum sp. in A. lacustris;

C. vianai and T. travnema in S. insculpta. This

result is possibly due to the fact that some

stretches of the Peixe River are still well

preserved and have suffered little human action.

This work expanded the geographic distribution

and registered new host for some nematode

species, contributing to the knowledge of the

biodiversity of parasites nematodes of fishes in

the São Paulo State.

Vanessa D. Abdallah was supported by a student

fellowship from FAPESP (2009/51726-6),

Rodney K. de Azevedo was supported by a

student fellowship from FAPESP (2010/06564-

5), Edmir Daniel de Carvalho was supported by a

Research fellowship from CNPq (107491/2009-

5) and Reinaldo José da Silva was supported by a

Research fellowship from CNPq (312590/2009-

1) and FAPESP (2009/53316-0). To students and

researches Franceschini L., Kurchevski G,

Ramos IP, Silva LAF, Sousa JQ, Souza DF,

Wunderlich AL, Zago A, Zanattta A and Zica

EOP for their assintance in the field.

ACKNOWLEDGMENTS

DISCUSSION

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*Author for correspondence / Autor para

correspondencia:

Vanessa Doro Abdallah

UNESP- Univ Estadual Paulista, Campus de

Botucatu, Instituto de Biociências, Departamento

de Parasitologia, Botucatu, São Paulo, Brazil.

E-mail/ correo electrónico:

vanessaabdallah@ig.com.br

Received December 1, 2011.

Accepted January 27, 2012.

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