ORIGINAL ARTICLE /ARTÍCULO ORIGINAL

THE MORPHOLOGY OF TEREANCISTRUM PARANAENSIS (DACTYLOGYRIDAE)

INFECTING SCHIZODON INTERMEDIUS, WITH A KEY TO THE SPECIES

NUEVOS DATOS EN LA MORFOLOGÍA DE TEREANCISTRUM PARANAENSIS

(DACTYLOGYRIDAE) INFECTANDO SCHIZODON INTERMEDIUS CON LA

INCLUSIÓN DE UNA CLAVE PARA EL GÉNERO

NOVOS DADOS SOBRE A MORFOLOGIA DE TEREANCISTRUM PARANAENSIS

(DACTYLOGYRIDAE) INFECTANDO SCHIZODON INTERMEDIUS COM A INCLUSÃO

DE UMA CHAVE PARA O GÊNERO

1 1 2

Vanessa Doro Abdallah ; Rodney Kozlowiski de Azevedo ; Karina Gabriela Dias Alves ; Aline de Almeida

2 2 2

Camargo ; Diego Henrique Mirandola Dias Vieira & Reinaldo José da Silva

1 Universidade do Sagrado Coração – USC, Brasil.

2 UNESP- Universidade Estadual Paulista “Júlio de Mesquita Filho”, Brasil.

Corresponding author: Vanessa Doro Abdallah, Rua irmã Arminda, 10-50, Jardim Brasil, Bauru, São Paulo, Brasil, 17011-

160. E-mail: vanessaabdallahusc@gmail.com

Neotropical Helminthology, 2016, 10(1), ene-jun: 5-12.

ABSTRACT

Keywords: Monogenea - morphologic analysis - Paraná river - piava - Trematoda - Veados river

The occurrence and new morphological data of Tereancistrum paranaensis Karling, Lopes,

Takemoto & Pavanelli, 2014 from the gills of Schizodon intermedius Garavello and Britski, 1990

in the Veados river, Municipality of Itatinga, São Paulo State, Brazil are reported. Our specimens

vary from those previously described in the following structures: ventral and dorsal bars,

prostatic reservoir and vagina. Moreover, the measurements of specimens collected in this study,

show differences from specimens collected from Paraná river floodplain. This is the first record

of T. paranaensis in São Paulo State, with S. borellii as new host. A key to species of this genus is

included.

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

RESUMO

Palavras-chave: Análise morfológica – Monogenea – piava – rio Paraná – rio Veados – Trematoda.

Neste trabalho, registramos a ocorrência e novos dados morfológicos de Tereancistrum

paranaensis Karling, Lopes, Takemoto & Pavanelli, 2014 coletados das brânquias de Schizodon

intermedius Garavello and Britski, 1990 do rio dos Veados, município de Itatinga, Estado de São

Paulo, Brasil. Nossos espécimes apresentam diferenças em relação aos espécimes previamente

descritos nas seguintes estruturas: barras Ventral e Dorsal, reservatório prostático e vagina. Além

disso, as medidas dos espécimes coletados neste estudo apresentam algumas diferenças em

relação aos espécimes coletados na planície de inundação do rio Paraná. Este é o primeiro

registro de T. paranaensis no Estado de São Paulo, com S. borellii como um novo hospedeiro.

Uma chave para as espécies deste gênero foi incluída.

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Abdallah et al.

INTRODUCTION

Despite the importance of Monogenea in

pisciculture, this group of parasites is not well

known in Brazil (Kohn & Santos, 1989).

Currently in according to Cohen et al. (2013)

the total number of monogenean species

known in Brazil is 437. Based on the limited

knowledge of the richness of the group, the

studies of the taxonomy of Monogenea are still

essential.

The Jurumirim dam is the first reservoir in

cascade of Paranapanema River, and operates

as a reservoir for regulating other downstream.

The reservoir was built in the late 1950 and

began in operation in 1962 (Henry &

Nogueira, 1999). Its drainage area covers

17,800 km , having ten tributaries on its right

margin and seven on the left margin (Carvalho,

2009). The Veados river is located in the

following geographical coordinates

(23º15'42.4''S; 48°37'27.6''W).

The genus Tereancistrum Kritsky, Thatcher &

Kayton (1980) includes Neotropical fish

parasites and is characterized mainly by

presenting spatulate sclerites associated with

the ventral anchors (Kristsky et al., 1980). To

date, eight species of this genus were recorded

parasitizing the gills of Neotropical fishes:

Tereancistrum kerri (Kritsky et al., 1980),

1980 in Brycon melanopterus (Cope, 1872),

Tereancistrum ornatus (Kritsky et al., 1980) in

Prochilodus reticulatus (Valenciennes, 1850),

Tereancistrum parvus (Kritsky et al., 1980), in

Leporinus fasciatus (Bloch, 1794)

Tereancistrum toksonum (Lizama et al., 2004)

and Tereancistrum curimba (Lizama et al.,

2004) in Prochilodus lineatus (Valenciennes,

1837), Tereancistrum arcuatus (Cohen et al.,

2012) in Salminus brasiliensis (Cuvier, 1816),

Tereancistrum pirassununguensis (Cepeda et

al., 2012) in Prochilodus lineatus and

Tereancistrum paranaensis (Karling et al.,

2014) in Schizodon borellii (Boulenger, 1900).

Schizodon intermedius (Boulenger 1900),

popularly known as “piava”, is a fish of the

order Characiformes. Its distribution area

comprises the South America: Upper Paraná

River basin (Froese & Pauly, 2010). This

species is classified in red category of IUCN

(International Union for Conservation of

Nature) (IUCN, 2014).

In this paper, we provide new information on

the geographical location, new host, and

complementary morphological data on T.

paranaensis on the basis of specimens

collected in S. borellii and also a key for

identification of the species in this genus.

In 2012, 10 specimens of Schizodon

intermedius (Garavello & Britski, 1990) were

collected for the study of monogeneans from

the Veados river (23º15'42.4''S; 48°37'27.6''W)

in the municipality of Itatinga, São Paulo State,

Brazil, under number collection license

DEFOP 96/1988. Fish were collected using

nylon monofilament gill nets with mesh sizes

of 3 to 14 cm at 3 sites on the river. The nets

were deployed at 1700 and removed at 0700

the following day for a total exposure time of

14 h. Each fish was placed in separate plastic

bags and kept in coolers until necropsy. The

gills were removed and the gill arches were

separated, then placed in a vial and flooded

with hot water (60° C to 70° C). The vial was

vigorously shaken to detach parasites from the

gills. After 1 h, absolute alcohol was added to

the vials in order to fix the monogeneans.

Some specimens were stained with Gomori's

trichrome and mounted with Canada balsam

and others were mounted using Gray and Wess'

medium (Humason, 1979) for the study of

sclerotized structures. Differential

interference contrast microscopy (Leica

DMLB 5000, Leica Microsystems, Wetzlar,

MATERIAL AND METHODS

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

Germany) was used for the morphologic

examination. Measurements were obtained

using a computerized image analysis system

(LAS V3.8, Leica Microsystems).

Measurements (in micrometers) were

expressed as the mean followed by the range in

parentheses. The illustrations were made with

the aid of a camera lucida mounted on a Leica

DMLS microscope. Voucher helminth

specimens were deposited at Coleção

Helmintológica do Instituto de Biociências de

Botucatu (CHIBB), Botucatu, São Paulo,

Brazil.

Dactylogyridae (Bychowsky, 1933)

Ancyrocephaline (Bychowsky, 1937)

Tereancistrum (Kritsky et al., 1980)

Tereancistrum paranaensis (Figures 1 and 2)

Morphological description (based on 8 whole-

mounted worms, 2 stained with Gomori's

trichrome and 6 mounted using Gray and Wess'

medium). Body 403 (303–587) long, elongate,

fusiform; 100 (82–121) wide near gonad level.

Tegument smooth. Cephalic lobes poorly

developed; head organs well developed. Eyes

two; component granules subspherical.

Pharynx spherical, 28 (27–30) in diameter;

esophagus short; intestinal ceca confluent

posterior to testis. Peduncle short; haptor

subhexagonal 71 (56–87) long, 94 (79–113)

wide. Hooks 24 (22–27) long, with erect

thumb, curved shaft, short point, dilated

proximal portion of shank; FH loop 0.3 shank

length. Ventral anchor robust 44 (37–53) long,

with well-developed superficial root and

incipient deep root, broadly curved shaft and

point, base 15 (12–18) wide. Accessory anchor

sclerite 24 (22-26) long, robust, with spatulate

end, connected to well-developed

musculature. Dorsal anchor 24 (21–31) long,

with superficial root more developed than deep

root, broadly curved shaft and point, base 7

(6–8) wide. Ventral bar 59 (55–62) long,

straight with rounded ends directed

posteriorly, with median groove. Dorsal bar 19

(16–21) long, straight with rounded ends

directed anteriorly. Gonads intercecal, slightly

overlapping. Testis elongate ovate; seminal

vesicle a simple dilation of vas deferens;

prostatic reservoir saccate. Male copulatory

organ tapered, tubular, coiled, with 2½

clockwise rings; ring diameter 14 (13-16).

Accessory piece 15 (13-17) long, variable, not

articulated with base of MCO. Germarium

elongate; vagina sinistral, forming simple

sclerotised tube; seminal receptacle spherical.

Vitellaria dense, random in trunk except in

regions of reproductive organs.

Host: Schizodon intermedius (Garavello &

Britski, 1990) (Characiformes: Anostomidae).

Site of infestation: Gills.

Locality: Veados river (23º15'42.4''S;

48°37'27.6''W), municipality of Itatinga, São

Paulo State, Brazil.

Specimens deposited: CHIBB 136L and 137L.

Prevalence of infestation: 1 of 10 specimens

analyzed (10%)

Key to known species of Tereancistrum

1. MCO non-coiled, unequal-sized hooks

………....................................................….. 2

-. MCO coiled, equal-sized hooks…..............3

2. Dorsal bar U-shaped.............Tereancistrum

kerri

-. Dorsal bar straight.........................................

....................................Tereancistrum arcuatus

3. Accessory piece articulated with the MCO

base............................. Tereancistrum ornatus

-. Accessory piece non-articulated with the

MCO base......................................................4

4 . M C O w i t h c l o c k w i s e

rings......................Tereancistrum paranaensis

-. MCO with counterclockwise rings..............5

5 . S l i g h t l y u n d u l a t e d v e n t r a l

bar................................. Tereancistrum parvus

- . O t h e r w i s e v e n t r a l

bar..................................................................6

6 . M C O w i t h 2

RESULTS

Morphology of Tereancistrum paranaensis

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Abdallah et al.

rings.................................................................

....................Tereancistrum pirassununguensis

-. MCO with 1¼ rings.................................…7

7. Presence of sclerotised intermuscular

structure between the accessory sclerites of the

ventral anchors ......….Tereancistrum curimba

-. Absence of a sclerotised intermuscular

structure between the accessory sclerites of the

ventral anchors ……. Tereancistrum toksonum

Figure 1. Tereancistrum paranaensis (A) Whole worm, ventral view. (B) Ventral bar. (C) Dorsal anchor. (D) Dorsal bar. (E)

Hook. (F) Ventral anchor and accessory anchor sclerite. (G) Vagina. (H) Male copulatory complex: MCO and accessory piece.

Scale bars: A, 100µm; B-F, 20 µm; G-H, 10 µm.

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

Morphology of Tereancistrum paranaensis

Figure 2. Tereancistrum paranaensis (A) Whole worm, ventral view. (B) Haptor showing ventral anchor, accessory anchor

sclerite, dorsal anchor, ventral bar and dorsal bar.

DISCUSSION

Our results showed new host and new

geographical location for T. paranaensis and

also that the specimens found in S. intermedius

from Veados river are slightly different in

comparison with the specimens collected in

the Paraná river floodplain by Karling et al.

(2014).

Karling et al. (2014) reported in T. paranaensis

an Ventral bar broadly M shaped and Dorsal

bar arc-shaped, whereas in our specimens the

Ventral bar is straight with rounded ends

directed posteriorly and Dorsal bar is straight

with rounded ends directed anteriorly. Karling

et al. (2014) described the prostatic reservoir

ovate; however, in our specimens this structure

is saccate. Furthermore, the vagina described

by Karling et al. (2014) is dextral but in

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Abdallah et al.

specimens collected in the present study the

vagina is sinistral.

Finally, the measurements of the specimens

collected in hosts from the Veados river present

some differences in relation to the specimens

described by Karling et al. (2014) (Table 1).

This may be related to intraspecific variations

that are common in Monogenea or to an

adaptive process (Kritsky et al., 1995). The

intraspecific morphometric and morphologic

changes are much common in parasites and

some authors comment that these changes may

be related to the different times of infection

and/or intense competition for space and other

host resources (Dobson, 1986; Shostak &

Dick, 1987; Szalai & Dick, 1989);

physiological differences found in different

hosts may affect the establishment, grow and

sexual maturity of the parasites (Watson &

Pike, 1993); specific polymorphism of the

parasites (Willis, 2002); different stages of

parasites development (Francisco et al., 2011)

and environmental variability (Gonzáles et al.,

2013).

In description of Karling et al. (2014), the

authors draw a well-developed muscle

structure connecting the sclerites accessories

of anchors but no mention is made in the

description. The prevalence found in this study

was much lower when compared to the

prevalence found in the study of Karling et al.

(2014), since only one analyzed fish was

parasitized. This structure was also observed in

our specimens. Finally we would like to

mention that these authors exchanged the

measurements of ventral and dorsal anchors in

the diagnosis, but in figure the identification

was correct. This is the first record of T.

paranaensis in southeastern Brazil, with S.

intermedius as new host, and also with

presentation of complementary data to the

morphology of this monogenean species.

Table 1. Comparative measurements of Tereancistrum paranaensis Karling et al., 2014 from Schizodon borellii

(Boulenger, 1900) and for specimens collected in this study (measurements in micrometers; mean followed by range

in parentheses; -, indicates no measurement available).

Measurements Karling et al. (2014)

n=10

Present study

n=8

Total variation

for the species

Body length 322.4 (247–360) 403 (303–587) 247-587

Body width

140.6 (76.8–216) 100 (82–121) 76.8–216

Pharynx diameter

20.9 (20.6–32.3) 28 (27–30) 20.6–32.3

Haptor length

71 (56–87) 56–87

Haptor width

94 (79–113) 79–113

Hook length

11.1 24 (22–27) 11.1–27

Ventral anchor length

44.6 (42–49.1) 44 (37–53) 37–53

Ventral anchor base

16.7 (14.7–18.6) 15 (12–18) 12–18.6

Accessory anchor sclerite

24 (22–26) 22–26

Dorsal anchor length

24.9 (20.8–28.4) 24 (21–31) 20.8–31

Dorsal anchor base

7.1 (5.9–7.8) 7 (6–8) 5.9–8

Ventral bar

54 (44.1–68.6) 59 (55–62) 44.1–68.6

Dorsal bar

18.3 (14.7–20.6) 19 (16–21) 14.7–21

Accessory piece length __ 15 (13–17) 13–17

MCO ring diameter 18.3 (15.7–20.6) 14 (13–16) 13–20.6

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

ACKNOWLEDGMENTS

Financial support: 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), and

Reinaldo José da Silva was supported by a

Research fellowship from CAPES (AUX-PE-

PNPD 3005/2010), FAPESP (2009/53316-0)

and CNPq (307808/2014-9). Diego H. M. D.

Vieira was supported by a student fellowship

from FAPESP (2011/22292-8). Authors would

like to thank to Elisa Pinto de Oliveira for

editing the English.

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