The silverside (Odonthestes argentinensis Valenciennes, 1835) is an important aquatic resource in coasts

of de la Plata River both in Argentina and Uruguay. This fish species acts as intermediate host of several

parasites, included trematode metacercariae. It was found in gills of silversides collected in Uruguayan

waters, metacercariae of Ascocotyle sp. Looss, 1899 (Heterophyidae) and Stephanoprora uruguayensis

Holcman-Spector & Olagüe, 1989 (Echinostomatidae). The aim of this study was determinate the

prevalence and mean intensity of digenean metacercariae in the gills of O. argentinensis from the

Uruguayan coast of de la Plata River, its relationship with fish size and sampling season, and to describe

the spatial distribution of that metacercariae in gills. A total of 279 fish were examined. The prevalence

and mean intensity of the parasites was 53.04% and 26.38 respectively for S. uruguayensis and 34.05%

and 11.38 for Ascocotyle sp. We found a different distribution in the metacercariae between fore and rear

gill arches. While S. uruguayensis is distributed mainly in the gills archs 1 and 2; Ascocotyle sp. are mainly

in the gills archs 3 and 4. Although S. uruguayensis metacercariae were mainly found in the proximal

region of the gill filament, (K-S = 4.80; p<0.01) and Ascocotyle sp., which was mainly present in the distal

region (K-S =4.89; p<0.01). This restriction of transverse and lateral niche may correspond to different

penetration route and the different size of the cercariae.

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

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

SPATIAL DISTRIBUTION OF TWO DIGENEA METACERCARIAE IN GILLS OF THE SILVERSIDE

ODONTESTHES ARGENTINENSIS (ATHERINIFORMES) FROM DE LA PLATA RIVER (URUGUAY,

SOUTHWESTERN ATLANTIC OCEAN)

DISTRIBUCIÓN ESPACIAL DE DOS METACERCARIAS DE DIGENEOS EN BRANQUIAS DEL

PEJERREY ODONTHESTES ARGENTINENSIS (ATHERINIFORMES) DEL RIO DE LA PLATA

(URUGUAY)

1 Instituto de Investigaciones Pesquera, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay. Tomás

Basáñez 1160, PC:11300, Montevideo, Uruguay.

2 Departamento de Parasitología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay.

Corresponding author: E-mail: dcarnevia@gmail.com

1 2 1 1

Daniel Carnevia Guerrero ; Oscar Castro Di Falco ; Maite Letamendía Tourné & Alejandro Perretta Noschesi

ABSTRACT

Keywords: Ascocotyle – metacercariae – Stephanoprora – Odonthestes argentinensis

Neotropical Helminthology

Volume13,Number1(jan-jun2019)

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

Auspiciado por:

Neotropical Helminthology, 2019, 13(1), ene-jun:41-47.

INTRODUCTION

RESUMEN

Palabras clave: Ascocotyle – metacercarias – Stephanoprora – Odonthestes argentinensis

El pejerrey (Odonthestes argentinensis Valenciennes, 1835) es un importante recurso acuático en las

costas del Río de la Plata. Este pez actúa como huesped intermediario de varios parásitos incluyendo

metacercárias de trematodes. En las branquias de estos peces colectados en la costa uruguaya del Rio de la

Plata encontramos metacercárias de Ascocotyle sp. Looss, 1899 (Heterophiydae) y Stephanoprora

uruguayensis Holcman-Spector & Olagüe, 1989 (Echinostomatidae). El objeto de este trabajo fue

determinar la prevalencia e intensidad media de infestación, así como describir la distribución especial de

estas metacercarias en las branquias. Se examinaron 279 peces. La prevalencia e intensidad media de la

parasitosis fue de 34,05 % y 11,38 para Ascocotyle sp. y de 53,04% y 26,38 para S. uruguayensis.

Observamos una distribución desigual de las metacercarias entre los arcos branquiales internos y

externos. Mientras que S. uruguayensis se distribuye principalmente en los arcos branquiales 1 y 2;

Ascocotyle sp. es más abundante en los arcos branquiales 3 y 4. Además las metacercárias de S.

uruguayensis se encontraron principalmente en la región proximal del filamento branquial (KS = 4.80; p

<0.01) mientras que las de Ascocotyle sp. están principalmente en la región distal ( KS = 4,89; p <0,01).

Los autores postulan que esta restricción del nicho transversal y lateral puede corresponder a diferentes

vías de penetración y al diferente tamaño de las cercárias.

microhabitat within the host, and several niches

can be recognized within it. The selection of the

implantation site of parasites in the gills may

respond to several factors: water flows into the gill

chamber, availability of gill area for clamping

sheets, differences in blood flow in different areas

of gill arches, immunity level, etc. (Gutiérrez &

Martorelli, 1999a). There are few studies on spatial

distribution and interaction of parasites in the gills

of fish. Most of this works concerns the ecology of

parasitic monogeneans (Gutiérrez & Martorelli,

1999b, 1999c; Simková et al., 2000; Gutiérrez,

2001; Turgut et al., 2006; Soylu et al., 2010) and

copepods (Benz & Dupre, 1987; Bashirullah,

2000; Timi, 2003; Failla, 2012) and also exists few

researchs aimed in the spatial distribution of other

parasites as myxosporidia or Digenea (Nie, 1996;

Molnar, 2002; Tombi et al., 2010).

The objective of this study was determinate the

prevalence and mean intensity of digenean

metacercariae in the gills of O. argentinensis from

the Uruguayan coast of the Río de la Plata, its

relationship with fish size and sampling season,

and to describe the spatial distribution of that

metacercariae in gills.

The silverside Odontesthes argentinensis

Valenciennes, 1835; is distributed from the state of

Santa Catarina in Brazil, to Bahía Blanca in

Argentina, and is one of the species caught by

commercial and recreational fishermen in “de la

Plata” River. This fish acts as intermediate host of

several trematodes (Alarcos et al., 2010). In

Uruguay were identified two metacercariae in gills

of O. argentinensis: Stephanoprora uruguayensis

(Echinostomatidae) and Ascocotyle sp.

(Heterophyidae) (Letamendia et al., 2010;

Carnevia et al., 2012; Castro et al., 2012; Maidana

et al., 2012).

The niche separation facilitates the coexistence of

several species by reducing competition for

resources (Slagsvold & Wiebe, 2007). There is an

interaction between parasites that inhabit the same

host and constant competitive interaction leads to

niche diversification by segregation, eventually

causing site specificity. The mechanisms

responsible for niche restriction in parasites are

competition, predation, and reinforcement of

reproductive barriers (Rohde, 1979). The gills are a

Neotropical Helminthology, 2019, 13(1), ene-jun Carnevia Guerrero et al.

tested. For the analysis of differences in

infrapopulation of parasites between the gills

arches or arch sectors a nonparametric

Kolmogorov-Smirnov test was performed because

the data were not normally distributed (Zar, 2010).

We used the statistical software Statgraphic Plus

5.1 and significance level was established at

p<0.05.

Ethic aspects: The authors declare that all the

ethical aspects of the country and international

ones were fulfilled.

A total of 279 fish were examined, 60.2% of them

were collected in cold season and 39.8% in warm

season. The prevalence and mean intensity of the

parasites was 53.04% and 26.38 respectively for S.

uruguayensis and 34.05% and 11.38 for Ascocotyle

sp. Prevalence and mean intensity of S.

uruguayensis were no correlated with fish size

(p=0.08 and p=0.16, respectively). However the

prevalence and the mean intensity of Ascocotyle sp.

were correlated with fish size (p=0.01 and 0.03,

respectively). The prevalence for S. uruguayensis

and Ascocotyle sp. in warm season was 27.02% and

13.5% respectively, while in cold season was

70.65% and 48.5% respectively. There was a

difference between the prevalence in the warm and

cold season for both S. uruguayensis (Z =-7.15,

p<0.01) and Ascocotyle sp. (Z=-6.02, p<0.01). We

Monthly samplings were made during a year in

coasts of de la Plata River in Montevideo city

(56º07`W, 34º54`S), in each sampling a minimum

of 20 fishes were collected. The fishes were

obtained from an artisanal fisherman, already dead

and were transported refrigerated to the laboratory.

Each fish was measured and weighed, then

dissected and gill arches were removed. The arches

were numbered 1 to 4 in an anteroposterior

direction (considering the arches 1 and 2 as fore

and 3 and 4 as rear) and the blades of each gill arch

were divided into proximal and distal region (fig.

1). Each gill arch was observed under a light

microscope in fresh, and the number and location

of the parasites were recorded.

With analytical purposes was adopted the criteria

of two thermal seasons in de la Plata River estuary

proposed by Guerrero et al. (1997), this implies the

existence of a warm season (December to March)

with a mean surface temperature of 12°C in our

sampling site and a cold season (June to

September) with 22°C of mean surface

temperature in the same site. Prevalence and mean

intensity of parasitism were calculated according

to Bush et al. (1997). The relationship between the

mean intensity and prevalence with the fish size

was analyzed by a correlation test (fish were

divided into 7 classes respect to the total length). To

compare the prevalence between seasons the null

hypothesis of equal proportions by Z test was

MATERIAL AND METHODS

RESULTS

Neotropical Helminthology, 2019, 13(1), ene-jun Metacercariae in gills of Odontesthes

Figure 1. Diagram showing gill arches position in Odontesthes argentinensis (operculum removed) and division of gill arch in

proximal and distal region (P and D).

DISCUSSION

lower than A. longa (93.06) (Perretta et al., 2005;

Brock & Font, 2009; Galvan-Borja et al., 2010;

Shoaibi et al., 2010; Martorelli et al., 2012).

If well the existence of a positive correlation

between the prevalence and mean intensity of

metacercariae with the fish size has been reported

previously, it is still discussed; several authors

argue this existence by means a cumulative effects

and the increment of parasite penetration with the

increase of the body surface of the fishes (Coleman

& Travis, 1998; Yamada et al., 2007; Namba et al.,

2012), but on the other hand, Portes et al. (2013) for

example, do not found correlations between the

number of metacercariae of A. longa and the fish

size.

The high prevalence and intensity levels found in

the cold season in this study contrast the findings

made by others. Coleman & Travis (1998) found an

increased prevalence and intensity of infection to

Ascocotyle pachycystis Schroeder & Leigh, 1965;

metacercariae in the warm season, which was

explained by the lower survival of highly

parasitized fish (Cyprinodon variegatus Lacépède,

1803) during the winter, and by the low production

of cercariae by lowering the temperature

(Steinauer & Font, 2003). A possible explanation

of our findings could be that O. argentinensis

breeding in the cold season, many juveniles being

captured in the warm season, so the cumulative

effect is more pronounced during the cold season.

There is little information that allows us to interpret

the preferential location of Ascocotyle sp. and S.

uruguayensis in the gills of O.argentinensis. The

morphological and physiological factors that

determine the selection of a specific parasite are

still unknown for most species. In the case of the

gill parasites, differences in the flow of water

between gills, as well as differences in blood flow

found a different distribution in the metacercariae

between fore and rear gill arches. While S.

uruguayensis is distributed mainly in the gills archs

1 and 2; Ascocotyle sp. are mainly in the gills archs

3 and 4. Differences were found between the total

number of metacercariae of S. uruguayensis (K-S =

3.03; p<0.01) and Ascocotyle sp. (K-S = 1.82;

p<0.01) present in the gills 1 and 2 with respect to 3

and 4. Differences were found between the number

of metacercariae of S. uruguayensis (K-S = 4.80;

p<0.01), which were mainly found in the proximal

region of the gill filament, and Ascocotyle sp. (K-S

=4.89; p<0.01), which was mainly present in the

distal region (Table 1).

The prevalence of S. uruguayensis found in the

silverside (53.04%) was higher than that found in

other fish species in Patagonia (Galaxias

maculatus Jenyns, 1842, 29.54%, Brachygalaxias

bulbcki Regan, 1908. 26.9% , Aplochiton zebra

Jenyns, 1842, 3%) (Viozzi et al., 2008, 2009;

Fernández et al., 2012), but lesser than the

prevalence of S. aylacostoma Ostrowski &

Quintana, 2007; found in fishes from the Parana

River (88-100%) (Ostrowski & Quintana, 2007).

Instead the mean intensity of infection (26.38) was

much higher than that cited by these researchers (1

to 3.8).

The prevalence of Ascocotyle sp. found in this

study (34.05%) was lower than that found in other

fish species (A. longa Ransom,1920, 35%, A.

tenuicollis Price, 1935, 58%, A. ampullacea Miller

& Harkima, 1962, 80% and A. mcintoshi Price,

1936, 87%). The mean intensity of infection

(11.38) was similar to that reported for A.

ampullacea and A. mcintoshi (9.1 to 10.8) but

Neotropical Helminthology, 2019, 13(1), ene-jun Carnevia Guerrero et al.

Table 1. Metacercariae in the gills of Odontesthes argentinensis from Rio de la Plata, Uruguay (average, SD,

minimum-maximun) (n = 279).

site

Stephanoprora

uruguayensis Ascocotyle sp.

Gills arches 1 and 2

98.91 +

71.32 (1 –

308) 1.64 +

2.14 (0 – 8)

Gills arches 3 and 4

19.65 + 16.19 (1 –

62) 2.17 +

2.23 (0 – 8)

Proximal region of gills

56.32 +

62.31 (1 –

308) 0.32 +

1.08 (0 – 8)

Distal region of gills

2. 94 +

13.92 (0 –

113) 1.58 +

2.02 (0 – 7)

to areas of the gills, have been postulated as the

main factors that determine the preferential

localization (Rohde, 1979). We postulate a

preferential location of As co co ty le and

Stephanoprora metacercariae in gills of O.

argentinensis based on the different route of arrival

to the gill and different cercariae sizes (Ascocotyle

140-265 µm, Stephanoprora 85-141 µm).

According to Stein (1968) and Leigh (1974)

cercariae of the genus Ascocotyle penetrate

through the gills of fish, then migrate to the target

o r g a n s . B y c o n t r a s t , c e r c a r i a e o f

Echinostomatidae have a great tail and takes

intense movements near the surface to attract fish

that ingest, afterwards penetrate the wall gut and

would travel through the bloodstream to the target

organs. Gill would be reached via the branchial

artery afferent to settle at the secondary lamellae

(Koie, 1986; Paller & Uga, 2008).

Odontesthes argentinensis could be parasitized

with trematode metacercariae of the family

H e t e r o p h y i d a e ( A s c o c o t y l e s p . ) a n d

Echinostomatidae (Stephanoprora uruguayensis)

in gills, with higher prevalence and intensity of

infection in the cold season. Metacercariae are

differentially located in the gills: S. uruguayensis

dominates arches 1 and 2 in the proximal area,

while Ascocotyle sp. predominates in arches 3 and

4 in the distal zone. This restriction of transverse

and lateral niche may correspond to different

penetration route and the different size of the

cercariae.

To Florencia Cremonte for critically reading the

manuscript and appropriate suggestions.

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Neotropical Helminthology, 2019, 13(1), ene-jun Metacercariae in gills of Odontesthes