Macroparasites of silversides (Atherinopsidae: Odontesthes) in Argentina

Abstract

This study presents new geographical distribution records for the macroparasites of the marine Odontesthes nigricans (Richardson, 1848) (89 wild specimens), and for the freshwater silversides Odontesthes bonariensis (Valenciennes, 1835) (43 wild and 108 cultured specimens), and Odontesthes hatcheri (Eigenmann, 1909) (183 wild specimens) from Argentina. These data represent records of 12 parasite taxa for O. nigricans, 8 for O. bonariensis, and 19 for O. hatcheri, which include digeneans, monogeneans, cestodes, nematodes, acantocephalans, mollusks, copepods, and branchiurans. For cultured O. bonariensis, the records of the present study correspond to the first reports of parasites in the literature. This work provides also data on site of infection, parasite load, and development stages for the parasite species.

Resumen

Este estudio presenta nuevos registros de distribución geográfica de macroparásitos del pejerrey marino Odontesthes nigricans (Richardson, 1848) (89 especímenes silvestres), de los pejerreyes de agua dulce Odontesthes bonariensis (Valenciennes, 1835) (43 ejemplares silvestres y 108 cultivados) y de Odontesthes hatcheri (Eigenmann, 1909) (183 especímenes silvestres) en Argentina. Doce taxones parásitos se registraron para O. nigricans, 8 para O. bonariensis y 19 para O. hatcheri, incluyendo digéneos, monogéneos, cestodos, nematodos, acantocéfalos, moluscos, copépodos y branquiuros. Para los ejemplares de O. bonariensis de cultivo, los registros del presente estudio corresponden a los primeros sobre parásitos en la literatura. Además, se presentan datos sobre la localización del parásito, sus valores de infección y sus estados de desarrollo.

Introduction

The species of Odontesthes (silversides) compose the most representative genus of Atherinopsidae, containing 19 species (Dyer, 2006). The silversides have great adaptability to different habitats and are distributed in marine, brackish, and freshwater environments (Dyer, 2006). Due to the flavor of the meat, these fishes are important in recreational fishery, commercial exploitation, and aquaculture (Grosman, 2001). Odontesthes bonariensis (Valenciennes, 1835) is the only cultured species, and has been widely used for repopulation purposes and have been introduced into Europe, Asia, and Africa (Tombari & Volpedo, 2008).

In Argentina, studies on freshwater silversides are mainly focused on culture, genetics, physiology, and ecology of O. bonariensis (Colautti, Garcia, Balboni, & Baigún, 2010; Grosman, 2001), and of Odontesthes hatcheri (Eigenmann, 1909) (Ruiz, 2007). The information on the marine silversides is limited, based mainly on Odontesthes nigricans (Richardson, 1848) and focused on the physiology of the specimens (Lattuca et al., 2009).

Although silversides species are widely distributed, reports of parasites from wild fishes are scarce and scattered (Carballo, 2008; Carballo, Laurenti, & Cremonte, 2011; Carballo, Navone, & Cremonte, 2011; Carballo, Cremonte, Navone, & Timi, 2012; Drago, 2012; Mancini, Rodríguez, Prosperi, Salinas, & Bucco, 2006; Mancini et al., 2008; Ortubay, Semenas, Úbeda, Quaggiotto, & Viozzi, 1994). Besides publications on rearing silversides, there is no published information on their parasites (Tanzola, Semenas, & Viozzi, 2009). The objective of the present work is to report the macroparasite fauna of the wild marine O. nigricans and the wild freshwater O. bonariensis and O. hatcheri, and the cultured O. bonariensis.

Materials and methods

A total of 89 O. nigricans were collected from 2 marine sites, 151 O. bonariensis were collected from 5 sites, and 183 O. hatcheri were collected from 13 sites, both the latter from freshwater environments (Fig. 1; Table 1). The fish were captured using gill and seine nets. Cultured O. bonariensis were collected from outdoor man-made ponds and indoor fiberglass tanks located within the campus of INTECH (Instituto Tecnológico de Chascomús), which were supplied with underground waters, and from floating cages located in Lacombe and Chascomús Pampean Lakes (Fig. 1; Table 1). Specimens of O. hatcheri and O. bonariensis were transported fresh to the laboratory, and those of O. nigricans were slit opened and fixed in 5% formalin in the field. Fish were measured, and necropsied to examine fins, skin, eyes, gills, and all internal organs with the aid of a dissecting microscope. The parasites were collected, identified, and counted. Prevalence and mean intensity were calculated. New geographical record refers to the first date that a parasite is reported in a new biogeographic region, ecoregion or basin, and new host record refers to the first time that a parasite is cited for a new host species. Furthermore, we followed the classification proposed by Niewiadomska (2002) for the family Diplostomidae, who considered as valid the genera Diplostomum, Austrodiplostomum, Tylodelphys, and Dolichorchis. Measurements of specimens are given in μm. Voucher specimens of parasites were deposited in the Colección Helmintológica del Museo de La Plata, Argentina.

Figure 1.

Location of the sampling sites of the silversides and their geographical coordinates in Argentina.

Table 1.

Data of silversides, localities of collections, sample, date and size; ^§ cultured fish.

Host	Localities	Sample date	Sample size	Standard fish size (cm)
				Mean	Range
O. nigricans	Punta María	Nov. 2010	67	16.8	9–25
	Varela Bay	Sep. 2010
		Jan. 2011	22	22.1	18–25
		Mar. 2011
O. bonariensis	La Plata River	Sep. 2011	11	18.5	10–27
	Man-made Pond (INTECH) ^§	Nov. 2007	10	11.4	9–16
	Chascomús Pampean Lake^§	Mar. 2008	77	10.3	8–14
	Chascomús Pampean Lake	Mar. 2008	32	14.6	9–24
	Lacombe Pampean Lake^§	Nov. 2007	21	14	13–15
	Marimenuco Reservoir	Mar. 2001	7	14.0	3–31
	Neuquén River	Oct. 2011	5	26.7	24–30
	Piedra del Águila Reservoir	Feb.1999	1	38.0	38
	Caleufu River	Mar. 2006	3	7.0	6–8
	Pond in Villa la Angostura	Jan. 2007	2	2.7	2–3
	Carrilafquen Lake	Oct. 2005	10	21.1	20–22
O. hatcheri	Carrilafquen Chica Lake	Oct. 2004	58	14.6	8–30
		Aug. 2005
	Morenito Lake	Feb. 1999	10	25.4	17–31
		Nov. 2000
	Moreno Oeste Lake	Mar.1999	16	31.1	28–36
		Aug. 2000
	Lezana Lake	Dec.2010	31	6.9	6–9
		Jan.2011
	Epuyen Lake	Mar.2003	3	25.3	22–27
	Rivadavia Lake	Feb. 2011	27	12.8	6–18
	Musters Lake	Oct. 2012	10	29.8	27–32

Results

The data obtained represent 15 new geographical records and 2 new host records for O. nigricans (Fig. 2; Table 2); 2 new geographical records, 1 new host record (T. cardiophilus), and a new species (Gyrodactylus sp.) for O. bonariensis (Fig. 3; Table 3); and 24 new geographical records and 1 new host record (Steganoderma szidati) for O. hatcheri (Fig. 4; Table 4). Prevalence and mean intensity for each parasite species, which include digeneans, monogeneans, cestodes, nematodes, acantocephalans, mollusks, copepods and branchiurans, are given in Tables 2–4.

Figure 2.

Microphotographs of Odontesthes nigricans parasites. 1, Diplostomum sp.; 2, Lecithaster sp.; 3, Proctotrema bartolii; 4, anterior end of Acuariinae sp.; 5, posterior end of Acuariinae sp.; 6, anterior end of Cosmocephalus sp.; 7, posterior end of Cosmocephalus sp.; 8, anterior end of Contracaecum sp.; 9, posterior end of Contracaecum sp.; 10, anterior end of Hysterothylacium sp.; 11, posterior end of Hysterothylacium sp.; 12, anterior end of Cucullanus sp.; 13, posterior end of a Cucullanus sp. female; 14, posterior end of a Cucullanus sp. male; 15, forebody of Hypoechinorhynchus sp.; 16, Corynosoma sp.; 17, Caligus sp.; 18, Peniculus sp.

Table 2.

Parasites of Odontesthes nigricans with data on site of infection, parasitic stage, localities, prevalence (P), mean intensity (MI), voucher specimens (VS), and collection number (CN). A, adult; C, Cysthacanth; L3, Larva 3; M, Metacercaria. *New geographical record; ^¥new host record; ^§cultured fish.

Parasite	Site	Stage	Locality	P (%)	MI	VS-CN
Diplostomum sp.^¥	Lens	M	Varela*	8.6	8.0	MLP-He 7125
Lecithaster sp.	Intestine	A	Varela*	30.0	11.6	MLP-He 7126
Proctotrema bartolii	Intestine	A	Punta María*	48.4	16.5	MLP-He 7127
Acuariinae gen. et sp.^¥	Liver and abdominal cavity	L3	Punta María*	12.9	1.8	MLP-He 7128
			Varela	15.7	1.9
Cosmocephalus sp.	Liver and abdominal cavity	L3	Punta María*	9.7	4.0	MLP-He 7129
			Varela*	8.6	1.6
Contracaecum sp.	Abdominal cavity	L3	Varela*	1.4	1.0
Hysterothylacium sp.	Intestine	L3	Punta María	3.2	1.0	MLP-He 7130
Cucullanus sp.	Intestine	A	Varela*	2.9	1.0
Hypoechinorhynchus sp.	Intestine	A	Varela*	2.9	1.5	MLP-He 7131
			Punta María*	9.7	4.0
Corynosoma sp.	Mesenteries, liver	C	Varela*	7.1	1.0	MLP-He 7132
			Punta María*	35.5	3.4
Caligus rogercresseyi	Dorsal, caudal fins	A	Varela*	11.4	1.8	MLP-Cr 27001
			Punta María*	29.0	1.0
Peniculus sp.	Body surface, fins	A	Varela*	28.6	5.3	MLP-Cr 27002

Figure 3.

Microphotographs of Odontesthes bonariensis parasites. 19, Tylodelphys cardiophilus; 20, Gyrodactylus sp.; 21, escolex of Cangatiella macdonaghi; 22, proglotids of Cangatiella macdonaghi.

Table 3.

Parasites of Odontesthes bonariensis with data on site of infection, stage, localities, prevalence (P), mean intensity (MI), voucher specimens (VS), and collection number (CN);^§cultured fish; A, adult; L3, Larva 3; M, Metacercaria. *New geographical record; ^¥new host record.

Parasite	Site	Stage	Locality	P (%)	MI	VS-CN
Austrodiplostomum mordax	brain	M	Lacombe^§	100	13.8
Tylodelphys cardiophilus^¥	pericardic cavity	M	Lacombe^§*	28.5	1.3	MLP-He 7133
Ascocotyle sp.	heart	M	Chascomús^§	42.9	3.3
			Chascomús	31.3	10.6
Phagicola sp.	gills	M	Chascomús^§	5.2	2.0
Gyrodactylus sp.	gills and fins	A	fiberglass tanks	28.6	6.7	MLP-He 7134
			man made pond	60.0	3.4
			Chascomús^§	90.5	4.5
			Chascomús	31.3	10.6
Cangatiella macdonaghi	intestine	A	Lacombe^§	85.7	13.8
			Chascomús^§	10.4	9.1	MLP-He 7135
			Chascomús	96.9	66.7
Contracaecum sp.	abdominal cavity	L3	La Plata River	9.1	1.0
			Lacombe^§	14.3	1.7
			Chascomús^§	3.9	1.0
			Chascomús	25.0	1.6
Argulus sp.	tegument	A	Lacombe^§*	4.7	1.0

Figure 4.

Microphotographs of Odontesthes hatcheri parasites. 23, Austrodiplostomum mordax; 24, Steganoderma macrophallus; 25, Steganoderma szidati.

Table 4.

Parasites of Odontesthes hatcheri with data on site of infection, stage, localities, prevalence (P), mean intensity (MI), voucher specimens (VS), and collection number (CN); A, adult; G, Glochidium; L3, Larva 3; M, Metacercaria. *New geographical record; ^¥new host record.

Parasite	Site	Stage	Locality	P (%)	MI	VS-CN
Austrodiplostomum mordax	Brain	M	Carrilafquen Chica	50	6.3	MLP-He 7136
			El Chañar	60	5.0
			Marimenuco	14.3	41.0
Diplostomum sp.	Eyes	M	Musters	80	80.5
Tylodelphys barilochensis	Brain	M	Moreno	5.9	1.0
Tylodelphys cardiophilus	Pericardiccavity	M	Carrilafquen Chica	3.8	1.0	MLP-He 7137
Tylodelphys destructor	Brain	M	Carrilafquen Chica	17.0	1.0	MLP-He 7138
			El Chañar	40.0	2.0
Tylodelphys barilochensis	Brain	M	Morenito	6.3	4.0
			Epuyén	66.6	3.0
			Lezana	22.6	4.6
			Marimenuco	14.3	4.0
Stephanoprora uruguayense	Gills	M	El Chañar	100.0	57.4
			Marimenuco	42.9	2.3
Steganoderma macrophallus	Intestine	A	El Chañar	40.0	2.0	MLP-He 7139
			Musters	30.0	224.0
Steganoderma szidati	Intestine	A	Moreno	5.9	40.0	MLP-He 7140
Cangatiella macdonaghi	Intestine	A	El Chañar	80.0	10.8
			Marimenuco	57.1	4.5
			Morenito	43.8	20.3
			Moreno	64.7	27.7
			Musters	30.0	9.6
Contracaecum sp.	Intestinewall	L3	El Chañar	20.0	2.0
			Carrilafquen Chica	3.8	1.0
			Morenito	6.3	1.0
			Moreno	23.5	1.3
			Musters	40.0	2.0
			Caleufu	33.3	1.0
Hysterothylacium patagonense	Intestine	L4	Morenito	6.3	3.0
			Moreno	23.5	5.8
			Epuyen	33.3	1.0
Camallanus corderoi	Intestine	A	Marimenuco	42.9	1.3
			Morenito	31.3	18.8
			Moreno	47.0	12.1
			Lezana	3.2	1.0
			Musters	10.0	3.0
Acanthocephalus tumescens	Intestine	A	Carrilafquen Chica	14.3	3.7
			Morenito	6.3	2.0
			Rivadavia	11.1	3.7
Pomphorhynchus patagonicus	Intestine	A	Lezana	3.2	1.0
			Musters	90.0	12.8
Diplodon chilensis	Gills,fins	G	Carrilafquen	28.6	2.8
			Morenito	12.5	28.5
			Moreno	58.8	35.9
			Epuyen	100.0	13.6
			Rivadavia	22.2	2.8
Ergasilus sieboldi	Gills	A	Marimenuco	42.9	2.3
			El Chañar	40.0	3.0
			Piedra del Águila	100.0	2.0
			Morenito	56.3	6.0
			Moreno	88.2	19.7
			Musters	100.0	46.0

The marine silverside, O. nigricans, was parasitized by the digeneans Diplostomum sp., Lecithaster sp., Proctotrema bartoliiCarballo, Laurenti, & Cremonte, 2011. The following nematodes Acuariinae gen. et sp., Cosmocephalus sp., Contracaecum sp., Hysterothylacium sp. and Cucullanus sp., the acanthocephalans Hypoechinorhynchus sp. and Corynosoma sp., and the copepods Caligus rogercresseyi (Boxshall & Bravo, 2000) and Peniculus sp. were also recorded (Table 2). The specimens of Diplostomum were assigned to this genus since they are metacercariae of the “Diplostomulum” type (not encysted metacercariae), which were localized in the lens of fish. The metacercariae measured 260–701 in length × 144–326 width, had the anterior end of the body trilobate, with small lateral protuberances (lappets) on either side of the oral sucker (36–72 long × 36–65 wide); the ventral sucker (26–72 long × 29–65 wide) was located postequatorially and is similar in size to that of the oral sucker. Just behind the ventral sucker there is a longitudinal holdfast organ (65–168 long). The specimens of Lecithaster sp. collected presented a 4-lobed ovary and a vitellarium rosette-shaped with 7 lobes. The larvae 3 of Acuariinae gen. et sp. have well developed pseudolabia, but the lateral alae are absent, therefore they could not be assigned to any known genus. The Cucullanus specimens collected in this study (1 male and 2 immature females) have the deirids located in the first third of the esophagus (182–193 from the anterior end), absence of papillae anterior to ventral sucker, presence of gubernaculum, and spicules reaching anterior end of ventral sucker. Peniculus sp. have a cephalothorax of 454 long × 511 wide; a neck of 227–284 long, a trunk 3,550–4,658 long × 880–1,227 wide, a ratio length to wide trunk of 3.6–4.0, with 4 swimming legs, with 3 and 4 further apart from legs 1 and 2.

The freshwater silverside O. bonariensis was parasitized by metacercariae of Austrodiplostomum mordax Szidat and Nani, 1951, Tylodelphys cardiophilus Szidat, 1969, Ascocotyle sp., and Phagicola sp., the monogenean Gyrodactylus sp., the cestode Cangatiella macdonaghi (Szidat & Nani, 1951), the nematode Contracaecum sp., and the branchiuran Argulus sp. (Table 3). Odontesthes hatcheri was parasitized by the digeneans A. mordax, Diplostomum sp., Tylodelphys barilochensis Quaggiotto and Valverde, 1992, T. cardiophilus, Tylodelphys destructor Szidat and Nani, 1951, Ascocotyle sp., Phagicola sp., Stephanoprora uruguayense Holcman-Spector and Olagüe, 1989, Steganoderma macrophallus Szidat and Nani, 1951, and Steganoderma szidati Viozzi, Flores and Ostrowski de Núñez, 2000, the cestodes C. macdonaghi, the nematodes Contracaecum sp., Hysterothylacium patagonense Moravec, Urawa and Coria, 1997, and Camallanus corderoi Torres, Teuber and Miranda, 1990, the acanthocephalans Acanthocephalus tumescens (von Linstow, 1896) and Pomphorhynchus patagonicus Ortubay, Úbeda, Semenas and Kennedy, 1991, the mollusk Diplodon chilensis Gray, 1828 and the copepod Ergasilus sieboldi von Nordman, 1832 (Table 4). As mentioned above, the metacercariae collected from the lens of O. hatcheri, which were the diplostomulum type were assigned to the genus Diplostomum. They measured 509–701 in length × 259–336 width. They also had the anterior end of the body trilobate, with small lateral lappets on either side of the oral sucker (53–82 long × 48–72 wide); the ventral sucker (36–60 long × 43–60 wide) is oval to round, located postequatorially and similar in size to that of the oral sucker. Just posterior to ventral sucker is the holdfast organ (96–144 long).

For cultured O. bonariensis, the parasite richness was 1 parasite species (Gyrodactylus sp.) taken from samples from indoor fiberglass tanks, and for those cultured outdoor in man-made ponds, 5 species (A. mordax, T. cardiophilus, C. macdonaghi, Contracaecum sp., and Argulus sp.) for fish reared in cages of Lacombe Pampean Lake, and also 5 species (Ascocotyle sp., Phagicola sp., Gyrodactylus sp., C. macdonaghi, and Contracaecum sp.) for those collected from cages of Chascomús Pampean Lake (Table 3).

Discussion

Specimens belonging to Digenea, Monogenea, Cestoda, Nematoda, Acanthocephala, Mollusca, Copepoda, and Branchiura are reported herein. Since larvae were the most common stages found in previous as well as, in the present work, the taxonomic identification at species level is difficult, considering that many of these parasites and their life cycles are not yet elucidated. All records reported in this study represent 41 new geographical records, 4 new host records and 1 new parasite species.

For O. nigricans, the parasites Diplostomum sp. and Acuariinae gen. et sp. were reported for the first time, and Cucullanus sp. may be a new parasite species. With regard to the Diplostomum metacercaria, we assumed that the metacercariae of O. nigricans and O. hatcheri belong to the same species as they show similar morphometric characteristics. Diplostomum species that have been found in the Antarctic region are D. minutum Szidat, 1964; D. antarcticum Freiler, 1986; and D. dominicanum Freiler, 1986 recorded from the kelp gull Larus dominicanus (González-Acuña et al., 2009). The metacercariae of Diplostomum found in O. nigricans and O. hatcheri could possibly correspond to D. minutum since adults of this species have been reported in L. dominicanus in Chubut and in Antarctica (Niewiadomska, Zdzitowiecki, & Ostrowski-de Núñez, 1989), near the site of the present study. It has been pointed out that lens metacercariae of Diplostomum have a low specificity (Locke et al., 2015), so the marine silverside could be infected with cercariae of Diplostomum when they ascend the rivers in the Magellan Strait (Dyer, 2000).

Lecithaster australis Prudhoe and Bray, 1973 and L. micropsiZdzitowiecki, 1992 were recorded in several species of nothotenids and gadiids in the South West Atlantic Ocean (Suriano & Sutton, 1981; Zdzitowiecki, 1992). The specimens of Lecithaster collected in the present study could not be assigned to any of those species, due to morphometric differences with the known species. The specimens are similar to those collected from O. nigricans and O. smitti in Nuevo and San José Gulfs, Chubut Province (Argentina), but the identification has not been determined (Carballo, 2008). The larva 3 of Cosmocephalus sp. most likely belongs to Cosmocephalus obvelatus (Creplin, 1825), since this species was recovered in the Chubut Province from O. nigricans parasitizing the same infection site (Carballo, Navone, et al., 2011). Four Cucullanus species have been described in the Argentinean Sea. Cucullanus marplatensisDaniel, Timi, and Sardella, 2002 was reported for Odontesthes species (Carballo, Laurenti, et al., 2011; Daniel et al., 2002). The Cucullanus specimens collected in this study differ from all the species of Cucullanus reported in Argentinean Sea. This finding would constitute a new parasite species. Peniculus fistula von Nordmann, 1832 was first recorded in the Strait of Magellan in an unknown host (Stuardo & Fagetti, 1961). Later, Peniculus sp. was registered in O. nigricans and O. smitti in the North Patagonian Gulfs (Carballo, Navone, et al., 2011). The specimens recovered in this work from O. nigricans, have a smaller length to width ratio (3.6–4.0) than P. fistula, which shows a trunk more than 6 times longer than wide (Alexander, 1983). They are similar to P. ostraciontis Yamaguti, 1939 and P. truncates Shiino, 1956 considering the distribution of swimming legs; however, our specimens cannot be assigned to any of these species since they have an intermediate length to width ratio of the trunk (P. truncatus 3.3 and P. ostraciontis 4.3) (Alexander, 1983).

For cultured O. bonariensis, the records herein correspond to the first reports of any parasites. The species richness of silversides collected from floating cages of Lacombe and Chascomús Pampean Lakes, were similar to those collected from wild silversides (Drago, 2012). Although richness was similar between cultured and wild specimens of Lacombe Pampean Lake the composition of the parasite community was different, for example T. cardiophilus and Argulus sp. were found only in cultured fish, and Hysterothylacium sp. and Wolffhuggelia matercula only in wild fish (Drago, 2012). This difference can be attributed to the life cycle of the parasites, meanwhile T. cardiophilus and Argulus sp. are transmitted by motile larvae (cercariae and juveniles), Hysterothylacium sp. and W. matercula require the consumption of an infected crustacean which are not available for cultured fishes. Silversides cultured in cages, which are located in the Pampean Lakes, acquired parasites from the environment, being of interest to human health Contracaecum sp., which is zoonotic, and for fish health Gyrodactylus sp. and Argulus sp., which could be pathogenic for fish if intensities of infection are increased (Woo, 1995).

Both freshwater silversides species were parasitized by the diplostomids A. mordax and T. cardiophilus, and were recorded in 6 new localities. Besides, Tylodelphys sp., T. destructor, T. barilochensis and Diplostomum sp. were recorded for O. hatcheri in 8 new localities. Both freshwater silversides species were parasitized by the heterophyids Ascocotyle sp. and Phagicola sp. constituting 4 new localities, and by the cestodes C. macdonaghi representing 7 new localities. Finally, the anisakid larvae Contracaecum sp., were found in O. bonariensis and O. hatcheri, while Hysterothylacium sp. was found only in O. hatcheri; these findings constitute 12 new localities. The following parasites: S. uruguayense (2 records), S. macrophallus (2), S. szidati (1), C. corderoi (5), A. tumescens (3), P. patagonicus (2), and D. chilensis (5) were recovered in new localities for O. hatcheri; and Gyrodactylus sp. (1) and Argulus sp. (1) represent new localities for O. bonariensis. The copepod E. sieboldi was first reported in Patagonia for Percichthys trucha (Cuvier & Valenciennes) (Szidat, 1956). Additionally larval stages and male specimens of E. sieboldi were reported from an Andean Patagonian lake (Modenutti & Balseiro, 1989). According to Szidat (1956), the Patagonian specimens showed scarce differences with specimens from Europe. Our specimens showed no differences with those collected from P. trucha from Pellegrini Lake and Limay River (Szidat, 1956). As the identity is dubious, we prefer to be conservative and assigned them to E. sieboldi, but molecular studies are needed to confirm the identity of the specimens.

The specimens of O. nigricans collected in this study showed a similar richness value (12 species) than those collected in Nuevo and San José gulfs (13 species in both gulfs). Although differences in the composition of parasite communities were observed, both populations share P. bartolii, Lecisthaster sp., Cosmocephalus sp., Hypoechinorhynchus sp., and Corynosoma sp., and differ in the presence of Diplostomum sp., Hysterothylacium sp., and C. rogercresseyi found in this study, and Prosorhynchoides sp., Huffmanela moraveci Carballo and Navone, 2007, Anisakis sp., Pseudoterranova sp., and Bomolochus globiceps (Vervoort and Ramírez, 1968) which were found only in the North Patagonian gulfs (Carballo, Navone, et al., 2011). These differences could be attributed to the fact that Nuevo and San José gulfs are in the ecotone between the Argentine and Patagonian ichthyogeographical provinces, while our samples were collected in Tierra del Fuego, in the southernmost part of Patagonian province. Although O. bonariensis and O. hatcheri were collected from 2 different ichthyogeographical provinces, Paranoplatensean Province and Patagonian Province, respectively; both share the metacercariae of A. mordax and T. cardiophilus and the cestode C. macdonaghi. The species of Odontesthes are mainly intermediate hosts for larval stages of Digenea and Nematoda, indicating that silversides in freshwater and marine environments are predominantly prey in the food chains.

Acknowledgements

To C. Luizon, G. Somoza, L. Miranda, and D. Collauti for their help in the collection of O. nigricans and O. bonariensis. We are grateful to Nahuel Huapi National Park authorities for sampling permissions. Financial support was provided by UNCo Grant (B-187), PIP 112-200801-01738 CONICET; and PICT BICENTENARIO N°1293 Agencia de Promoción Científica y Técnica.