RESEARCH NOTE/NOTA CIENTÍFICA

CUCULLANUS (CUCULLANUS) PINNAI PINNAI PARASITE OF RHAMDIOGLANIS

FRENATUS (SILURIFORMES, HEPTAPTERIDAE) IN A COASTAL STREAM OF

ATLANTIC FOREST, BRAZIL

CUCULLANUS (CUCULLANUS) PINNAI PINNAI PARÁSITO DE RHAMDIOGLANIS

FRENATUS (SILURIFORMES, HEPTAPTERIDAE) EN UN ARROYO COSTERO DE LA

MATA ATLÁNTICA, BRASIL

1* 1 1

Karine Soares de Oliveira , Larissa Jardim , João Alberto Paschoa dos Santos ,

2 2

Fábio Hideki Yamada & Reinaldo José da Silva

1Universidade Santa Cecília/UNISANTA, Laboratório de Peixes Continentais/LAPEC, Santos, São Paulo, Brazil.

*E-mail:kakabioroots@gmail.com

2Unesp - Univ Estadual Paulista, Instituto de Biociências, Campus de Botucatu, Departamento de Parasitologia, Laboratório

de Parasitologia de Animais Silvestres/LAPAS, Botucatu, São Paulo, Brazil

Neotropical Helminthology, 2015, 9(2), jul-dec: 351-357.

ABSTRACT

Keywords: Atlantic Forest - Cucullanidae - Freshwater Fish - Nematoda.

During surveys on helminth parasites of freshwater fishes from the Cubatão River, a new

occurrence of Cucullanus (Cucullanus) pinnai pinnai parasitizing Rhamdioglanis frenatus

(Siluriformes, Heptapteridae) was recorded. This nematode has been reported infecting several

host species from different localities, mainly Siluriformes and some Characiformes. The present

study is the first parasitological survey from R. frenatus and expands the range of fishes

parasitized with C. (C.) p. pinnai in the Neotropical region.

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

RESUMEN

Keywords: Cucullanidae - Mata Atlántica Nematoda - pez dulceacuicola.

Durante los estudios de helmintos parásitos de peces de agua dulce del arroyo Cubatão, se

registró una nueva ocurrencia de Cucullanus (Cucullanus) pinnai pinnai parasitando

Rhamdioglanis frenatus (Siluriformes, Heptapteridae). Este nematodo se ha registrado en varios

especies huéspedes de diferentes localidades, siendo la mayoría Siluriformes y algunos

Characiformes. El presente estudio es el primer estudio parasitológico de R. frenatus y amplía la

lista de peces parasitados por C. (Cucullanus) pinnai pinnai en la región Neotropical.

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INTRODUCTION

The Atlantic Forest is one of the main

biodiversity hotspots for conservation

priorities and highly threatened of the planet

(Myers et al., 2000). According to Colombo &

Joly (2010), this complex biome contains

higher biodiversity than most of the Amazon

forests. Therefore, there is only 7.6%, of the

original Atlantic Forest left, and less than 50%

of the remnants are protected in Conservation

Units (Colombo & Joly, 2010). “Serra do Mar”

is a mountain ridge covered by the Atlantic

Forest with many streams and high fish species

diversity estimated at 269 species belonging to

89 genera and 21 families (Abilhoa et al.,

2011).

Siluriformes Cuvier, 1817 comprises the most

morphologically diverse and geographically

widespread order of Ostariophysi with

approximately 36 families, 477 genera, and

3088 valid species (Ferraris, 2007). The catfish

family Heptapteridae Gil, 1861 is one of the

most diverse from Central and South America

(Rosas-Valdez & Pérez-Ponce de León, 2008).

Rhamdioglanis frenatus Ihering, 1907 lives in

streams with pools and riffles, bed sediments

of sand, gravel or rock on the bottom, and clear

water. This fish species is distributed from the

North of Santa Catarina State to South of Rio

de Janeiro State, Brazil (Menezes et al., 2007).

The Neotropical fauna of nematode parasites

from freshwater fish features more than 137

species and subspecies belonging to 52 genera

in 10 superfamilies. Cucullanidae Cobbold,

1864 is a large family of parasitic nematodes,

members of which have been described from

almost every part of the world (Ndew et al.,

2014). The cucullanids are peculiar intestinal

parasites of fishes and rarely turtles. Parasites

of this family are characterized by a highly

developed buccal cavity formed from the

oesophagus (i.e. oesophastome) (Berland,

1970). The genus Cucullanus Müller, 1777

includes approximately 100 species (Timi &

Lanfranchi, 2006). According to Giese et al.

(2010), there are 26 known Neotropical

species of Cucullanus reported in South

American, in which 16 species have been

described in Brazil. Originally, Cucullanus

(Cucullanus) pinnai pinnai Travassos, Artigas

& Pereira, 1928 was described from intestine

of Pimelodus clarias Linnaeus, 1758 and

Pseudoplatystoma sp. from the Paraná River,

São Paulo State, Brazil (Moravec et al., 1993).

The aim of this study was to report the new

occurrence of C. (C.) pinnai pinnai

parasitizing R. frenatus from Cubatão River,

São Paulo State, Brazil.

The Cubatão River has approximately 35 km

long and is located in the “Baixada Santista”

watershed. It occupies an area of 175.55 km

(Abreu-Santos et al., 2014) and is inserted in

the Conservation Unit of the “Parque Estadual

da Serra do Mar” (PESM), Itutinga Pilões. The

headwaters of the Cubatão River are located in

the city of São Bernardo do Campo, and that

finish discharging at Cubatão municipality,

São Paulo State, Brazil (Luiz-Silva et al.,

2002) (23º56'03.3" to 23º55'50.2"S and

46º31'31.1" to 46º31'10.8"W) (Figure 1). This

work was approved by the Brazilian Institute

of Environment (IBAMA) SISBIO N. 25826-

A total of 32 specimens of R. frenatus were

sampled in July 2013 and February 2014 from

Cubatão River using electrofishing. Fish were

fixed in 4% formalin and after, they were

necropsied and the organs were surveyed for

endoparasites. Nematodes found were stored

in 70% ethanol and diaphanized with lactic

acid or lactophenol. Identification of the C.

(Cucullanus) pinnai pinnai followed Moravec

(1998). All measurements are in micrometers

with the mean followed by the range and the

MATERIAL AND METHODS

Soares de Oliveira et al.

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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Cucullanus pinnai pinnai parasite of Rhamdioglanis

number of specimens measured between

parentheses. The images were made using a

differential interference contrast microscope

(Leica DM 5000B).

Phylum Nematoda Rudolphi, 1808

Class Secernentea Von Linstow, 1905

Order Ascaridida Skrjabin and Schulz, 1940

Family Cucullanidae Cobbold, 1864

Genus Cucullanus Müller, 1777

Cucullanus (Cucullanus) pinnai pinnai

Travassos, Artigas & Pereira, 1928

(Figure 2)

Diagnosis: Nematode medium size. Dorso-

ventral oral aperture surrounded by a cuticular

ring with an internal row of denticles, and two

pairs of submedial cephalic papillae. Muscular

esophagus expands until the anterior end to

form a pseudo oral capsule (esophastome).

Nerve ring surrounding esophagus near its

narrowest region. Excretory pore near but not

beyond posterior end of esophagus. Tails

pointed.

Female (based on 7 specimens): Body 4.16

(2.31 – 4.97, n=7) long; 0.27 (0.14 – 0.36, n=7)

wide. Esophagus 0.53 (0.44 – 0.59, n=7) long;

width 0.12 (0.10 – 0.14, n=7) in the anterior

portion and 0.11 (0.07 – 0.13, n=7) in posterior

portion. Cauda 0.17 (0.14 – 0.21, n=7) long.

Vulva with slightly projected lips 1.34 (0.96 –

2.30, n=5), and muscular vagina. Anus 0.02

RESULTS

Figure 1. Map of Cubatão River, municipality of Cubatão, São Paulo State, Brazil, showing the areas (A and B) of collection of

the Rhamdioglanis frenatus specimens included in this study.

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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Soares de Oliveira et al.

(0.02 – 0.04, n=7) from posterior end

extremity. Excretory pore 0.14 (0.26 – 0.39,

n=3) from anterior extremity. Conical tail.

Male (based on 9 specimens): Body 3.07 (2.47

– 3.57, n=9) long; 0.20 (0.17 – 0.22, n=9) wide.

Esophagus 0.47 (0.36 – 0.52, n=9) long; width

0.11 (0.083 – 0.14, n=9) in the anterior portion

and 0.09 (0.08 – 0.11, n=9) in posterior portion.

Caudal 0.16 (0.13 – 0.18, n=9) long. Tail tip

0.03 (0.03 – 0.05, n=9) long. Excretory pore

0.09 (0.23 – 0.29, n=3). Spicules equal and

sclerotized 0.45 (0.32 – 0.51, n=8) long.

Taxonomic summary

Type-host: Rhamdioglanis frenatus Ihering,

1907

Locality: Cubatão River, São Paulo State,

Brazil.

Site of infection: Intestine.

Prevalence: 31.25% (10 of 32 fishes

examined).

Mean Intensity of infection: 1.6 ± 4.24.

Figure 2. Cucullanus (Cucullanus) pinnai pinnai parasite of Rhamdioglanis frenatus in a coastal stream of Atlantic Forest,

Brazil. A) Anterior end, showing cephalic papillae (Cp), esophastome (Eso), nervous ring (Nr), and excretory pore (Ep). B)

Lateral view of the male posterior region, showing cloacal sucker (Cs), caudal papillae (Pa) gubernaculum (Gb), spicules (Sp),

and caudal tail (Ta). C) Detail of the vulvar region, showing vulva (Vu), muscular vagina (Va), and eggs (Eg). D) Lateral view of

the female posterior region, showing anus (An), and caudal tail (Ta).

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Table 1. Checklist of host species parasitized with Cucullanus (Cucullanus) pinnai pinnai and geographical

distribution from Neotropical region.

Host species Locality References

Ageneiosus valenciennesi Bleeker, 1864 Parana River -

Brazil Moravec et al.

(1993)

Galeocharax knerii Steindachner, 1879 Parana River -

Brazil Moravec et al. (1993)

Leporinus copelandii Steindachner, 1875 Mogi Guaçu River – Brazil Kohn & Fernandes (1987)

Loricaria sp. Mogi Guaçu River – Brazil Moravec et al. (1997)

Luciopimelodus pati Valenciennes, 1835 Parana River –

Argentina Moravec et al. (1993)

Megalonema platinum Günther, 1880 Parana River –

Uruguay Petter (1995)

Paulicea luetkeni Steindachner, 1876 Parana River -

Foz do Iguaçú Moravec et al. (1997)

Pimelodella gracilis Valenciennes, 1835 Parana River Brazil Moravec et al. (1997)

Pimelodus albicans Valenciennes, 1840 Parana River –

Argentina Chemes & Takemoto

(2011)

P. clarias Linnaeus, 1758 Parana River -

Brazil Kohn & Fernandes (1987)

P. maculatus Lacepède, 1803 Itaipu Reservoir -

Brazil Moravec et al. (1997)

P. ornatus Kner, 1858 Paraná River -

Brazil Moravec et al. (1993)

Pimelodus sp. Paraná River -

Brazil Moravec et al. (1993)

Pseudopimelodus roosevelti Borodin, 1927 Mogi Guaçu River - Brazil Kohn & Fernandes (1987)

Pseudoplatystoma sp. Parana River -

Brazil Moravec et al.

(1993)

P. coruscans Spix & Agassiz, 1829 Parana River -

Uruguay Petter (1995)

Rhamdioglanis frenatus, Ihering, 1907 Cubatão River -

Brazil Present study

Schizodon borellii Boulenger, 1900 Parana River -

Brazil Machado et al. (1994)

Steindachneridion parahybae Steindachner, 1877 Mogi Guaçu River - Brazil Kohn & Fernandes (1987)

Cucullanus (Cucullanus) pinnai pinnai have

been reported for several host species of

different localities (Eiras et al., 2010; Kohn et

al., 2011) (Table 1).

This finding represents the first record for

Cucullanus (Cucullanus) pinnai pinnai

parasiting R. frenatus from Cubatão River, São

Paulo State, Brazil and expands the

biogeography and occurrence of this nematode

species, corroborating Moreira et al. (2014),

that suggesting low specificity of this

nematode that has been reported parasitizing

several host species from Neotropical region.

According to Eiras et al. (2011), in the past two

decades the studies of parasite of freshwater

fishes has been focused mainly on fishes with

valuable resource. There is a lack of studies on

the parasite fauna of fishes from streams of

“Serra do Mar”. Furthermore, this paper

provides information of fish parasite from

stream of Atlantic forest one of the most

threatened Brazilian biome and that requires

conservation and sustainable policies.

The author thanks the Instituto Florestal for the

license granted for research (260108-

010.534/260108-010.525/260108-010.517),

along the Laboratório de Peixes Continentais

(LAPEC) and Laboratório de Parasitologia de

Animais Silvestres (LAPAS) for supporting

the study. Fabio Hideki Yamada thanks

Fundação de Amparo a Pesquisa do Estado de

São Paulo/FAPESP (2011/22603-3). Reinaldo

José da Silva is supported by CNPq

(307808/2014-9).

DISCUSSION

ACKNOWLEDGMENTS

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ucayalensis (Pisces: Auchenipteridae)

from Pará, Br azil . Journal of

Parasitology, vol. 96, pp. 389-394.

Kohn, A & Fernandes, BMM. 1987. Estudo

comparativos dos helmintos parasitos

de peixes do Rio Mogi Guassu, coletados

nas excursões realizadas entre 1927 e

1985. Mem. Inst. Oswaldo Cruz, Rio de

Janeiro, vol. 82, pp. 483-500.

Kohn, A, Moravec, F, Cohen, SC, Canzi, C,

Takemoto, RM & Fernandes, BMM.

2011. Helminths of freshwater fishes of

Itaipu, Brazil. Check List, vol. 7, pp.

681-690.

Luiz-Silva, W, Matos, RHR & Kristosch, GC.

2002. Geoquímica e índice de

geoacumulação de mercúrio em

sedimentos de superfície do estuário de

Santos-Cubatão (SP). Química Nova,

vol.5, pp. 753-756.

Machado, MH, Pavanelli, GC & Takemoto,

RM. 1994. Influence of host's sex and

size on endoparasitic infrapopulations

of Pseudoplatystoma corruscans and

Schizodon Borelli (Osteichthyes) of the

high Parana River, Brazil. Revista

Brasileira de Parasitolologia Veterinária,

vol. 3, pp.143-148.

Menezes, NA, Weitzman, SH, Oyakawa, OT,

Lima, FCT, Castro, RMC & Weitzman,

MJ. 2007. Peixes de água doce da Mata

Atlântica: lista preliminar das espécies e

comentários sobre conservação de

peixes de água doce neotropicais.

Museu de Zoologia, Universidade de

São Paulo, São Paulo.

Moravec, F. 1998. Nematodes of freshwater

fishes of the Neotropical Region.

Academia, Publishing House of the

Academy of Sciences of the Czech

Republic.

Moravec, F, Kohn, A & Fernandes, BMM.

1993. Nematode parasites of fishes of the

Par aná Riv er, Br azi l. Part 2.

S e u r a t o i d e a , A s c a r i d o i d e a ,

Habronematoidea and Acuarioidea.

Folia Parasitologica, vol. 40, pp. 115-

Abilhoa, V, Braga, RR, Bornatowski, H &

Vitule, JRS. 2011. Fishes of the Atlantic

Rain Forest Streams: Ecological

Patterns and Conservation. pp. 259-282.

In: Grillo, O & Venora, G, (eds.).

Changing Diversity in Changing

Environment. Croácia, InTech.

Abreu-Santos, B, Corrêa, PDT, Oyakawa, OT,

Santos, JAP & Schmiegelow, JMM.

2014. Fishes from the middle Cubatão

River drainage São Paulo State, Brazil.

Check List, vol. 10, pp. 1031-1035.

Berland, B. 1970. On the morphology of the

head in four species of Cucullanidae

(Nematoda). Sarsia, vol. 43, pp. 15-64.

Cheme, SB & Takemoto, RM. 2011. Diversity

of parasites from Middle Paraná system

f re s h w a t e r f i s h e s , A rg e n t i n a .

International Journal of Biodiversity and

Conservation, vol. 3, pp. 249-266.

Colombo, AF & Joly, CA. 2010. Brazilian

Atlantic Forest lato sensu: the most

ancient Brazilian forest, and a

biodiversity hotspot, is highly threatened

by climate change. Brazilian Journal of

Biology, vol. 70, pp. 697-708.

Eiras, JC, Takemoto, RM & Pavanelli GC.

2010. Diversidade dos parasitas de

peixes de água doce do Brasil. Maringá,

Chicletec.

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

Adriano, EA. 2011. About the

biodiversity of parasites of freshwater

fish from Brazil. Bulletin of the

European Association of Fish

Pathologists, vol. 31, pp. 161-168.

Ferraris Jr, CJ. 2007. Checklist of catfishes,

recent and fossil (Osteichthyes:

Siluriformes), and catalogue of

siluriform primary types. Zootaxa, vol.

1418, pp. 1-628.

Giese, EG, Furtado, AP, Lanfredi, RM &

Santos JN. 2010. A new cucullanid

species (Nematoda) from Ageneiosus

BIBLIOGRAPHIC REFERENCES

357

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Cucullanus pinnai pinnai parasite of Rhamdioglanis

134.

Moravec, F, Kohn, A & Fernandes, BMM.

1997. New observations on seuratoid

nematodes parasitic in fishes of the

P a r a n á R i v e r, B r a z i l . F o l i a

Parasitologica, vol. 44, pp. 209-223.

Moreira, LHA, Takemoto, RM, Pagotto, JPA &

Pavanelli, GC. 2014. Endoparasites

community structure of three fishes

species in tributary streams of the river

Pir a pó , Pa r an á s ta t e, B ra z il .

Neotropical Helminthology, vol. 8, pp.

97-109.

Myers, N, Mittermeier, RA, Mittermeier, CG,

Fonseca, GAB & Kent, J. 2000.

Biodiversity hotspots for conservation

priorities. Nature, vol. 403, pp. 853-858.

Ndew, DE, Diouf, M, Bâ, CT & Morand, S.

2014. A New Species of Cucullanus

( N e m a t o d a : C u c u l l a n i n a e ,

Cucullanidae) from Mugil curema

(Mugilidae) in Senegal (West Africa).

Comparative Parasitology, vol. 81, pp.

15-22.

Petter, AJ. 1995. Dichelyne moraveci n. sp.,

parasite de Pseudoplastystoma

fasciatum et notes sur les Cucullanidae

du Paraguay. Revue Suisse de Zoologie,

vol. 102, pp. 769-778.

Rosas-Valdez, R& Péres-Ponce de León, G.

2008. Composición taxonómica de los

helmintos parásitos de ictalúridos y

h e pt a p t é r i d o s ( O st e i c h t h y e s :

Suliriformes) de México, con una

hipótesis de homología biogeográfica

primaria. Revista Mexicana de

Biodiversidad, vol. 79, pp. 473-499.

Timi, JT & Lanfranchi, AL. 2006. A new

species of Cucullanus (Nematoda:

Cucullanidae) parasitizing Conger

orbignianus (Pisces: Congridae) from

Argentinean waters. Journal of

Parasitology, vol. 92, pp. 151-154.

Received April 17, 2015.

Accepted June 23, 2015.