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Infeccao por metacercarias de Austrodiplostomum compactum em peixes do Reservatorio de Nova Avanhandava, rio Tiete, Estado de Sao Paulo, Brasil.

Infection by Austrodiplostomum compactum metacercariae in fish from the Nova Avanhandava reservoir, Tiete river, Sao Paulo State, Brazil

Introduction

Digenetic helminthes of the family Diplostomidae are responsible for 'wormy cataract', also called diplostomiasis (MARTINS et al., 1999). The genus Austrodiplostomum Szidat and Nani, 1951 have been reported infecting several species of vertebrates (KOHN et al., 1995; RAMOS-RAMOS, 1995; YAMAGUTI, 1971; SCHOLTZ et al., 1995; NIEWIADOMSKA, 1996; NIEWIADOMSKA; LASKOWSKI, 2002). These parasites, when adults, are able to infect birds and mammals, and the metacercariae stage are found infecting fish and amphibians, which are intermediate hosts in their life cycle (AMATO et al., 2001; FLOWERS et al., 2004; OSTROWSKI-NUNEZ, 1982; RIETSCHEL; WERDING, 1978). According to Eiras (1994), the presence of this parasite in the eyes can cause blindness or reduced vision, making the fish susceptible to the predation that facilitates the transmission of the parasite to the definitive host.

Austrodiplostomum compactum (Lutz, 1928) metacercariae occur in the eyes of a wide variety of fish species (YAMADA et al., 2008). In Brazil, metacercariae infection by A. compactum has been registered in fish species in different hydrographic basins: Plagioscion squamosissimus (Heckel, 1840), Hoplias aff. malabaricus (Bloch, 1794), Cichla monoculus Spix, 1831 and Cichla ocellaris Bloch and Schneider, 1801, Satanoperca pappaterra (Heckel, 1840), Crenicichla britskii Kullander, 1982, Cichlasoma paranaense Kullander, 1983, Geophagus brasiliensis Quoy and Gaimard, 1824, Serrasalmus maculatus (Kner, 1858), Hypostomus regani (Ihering, 1905), Schizodon borellii (Boulenger, 1900) and Auchenipterus osteomystax Miranda-Ribeiro, 1918 (KOHN et al., 1995; MACHADO et al., 2005; MARTINS et al., 1999; 2002; NOVAES et al., 2006; PAES et al., 2003; PAVANELLI et al., 1997; SANTOS et al., 2002; YAMADA et al., 2007; YAMADA et al., 2008; ZICA et al., 2009).

Since the occurrence of A. compactum metacercariae was previously reported in the Tiete river (NOVAES et al., 2006; PAES et al., 2003) and considering the diversity of fish in the Tiete basin (VIDOTTO; CARVALHO, 2007) and the lack of parasitological studies in this environment highly influenced by human actions, the aim of this study was to evaluate the occurrence of these metacercariae in fish from the Santa Barbara river in the Nova Avanhandava reservoir, low Tiete river, Sao Paulo State, Brazil.

Material and methods

The study was conducted in the Santa Barbara river, municipality of Buritama, Sao Paulo State, Brazil, a major tributary of the Nova Avanhandava reservoir, the penultimate hydroelectric plant of the mid Tiete river, whose dam is located at the geographic coordinates 21[degrees]07'S and 50[degrees]17'W (Figure 1).

[FIGURE 1 OMITTED]

Fish were collected for this study on July 31, September 9, October 15 and December 18, 2003 using a gillnet of nylon monofilament, installed in several parts of the study area. Fish were identified and conferred on the basis of Reis et al. (2003) and Graca and Pavanelli (2007). For the determination of the hosts for A. compactum, each sampled fish was macroscopically examined for detection of the metacercariae in the ocular globe (aqueous and vitreous humor). When a parasite was observed in a fish species, the eyes of all specimens of this species were analyzed in a stereomicroscope.

The parasites collected were processed according to Amato et al. (1991). The morphometric analysis was performed using a computerized system for analysis of images QWin Lite 2.5 (Leica) in a sample of 21 metacercariae from P. squamosissimus. The morphometric results (in micrometers) are presented as minimum-maximum (mean) values.

The identification of the metacercariae was according to Niewiadomska (2002a; 2002b), Kohn et al. (1995), Santos et al. (2002), Novaes et al. (2006), and Zica et al. (2009). Voucher specimens were deposited in the Colecao Helmintologica of the Departamento de Parasitologia, Instituto de Biociencias, Universidade Estadual Paulista, Botucatu, Sao Paulo State, Brazil.

Prevalence, mean intensity of infection and abundance of infected fish was calculated according to Bush et al. (1997).

Results

In this study, 22 species of fish were recorded in the Nova Avanhandava reservoir: Acestrorhynchus lacustris (Lutken, 1875) (n = 1), Apareiodon affnis (Steindachner, 1879) (n = 19), Astyanax altiparanae Garutti and Britski, 2000 (n = 356), Astyanax fasciatus (Cuvier, 1819) (n = 1), Brycon orbignyanus (Valenciennes, 1850) (n = 2), Cichla kelberi (Kullander and Ferreira, 2006) (n = 7), Cichla piquiti (Kullander and Ferreira, 2006) (n = 3), Crenicichla britskii (n = 2), Hoplias malabaricus (n = 7), Hoplosternum littorale (Hancock, 1828) (n = 1), Hypostomus iheringii (Regan, 1908) (n = 3), Leporinus friderici (Bloch, 1794) (n = 5), Metynnis maculatus (Kner, 1858) (n = 298), Moenkhausia intermedia Eigenmann, 1908 (n = 14), Plagioscion squamosissimus (n = 213), Prochilodus lineatus (Valenciennes, 1836) (n = 1), Rhamdia quelen (Quoy and Gaimard, 1824) (n = 8), Satanoperca pappaterra (Heckel, 1840) (n = 25), Schizodon nasutus Kner, 1859 (n = 84), Serrasalmus maculatus (n = 68), Steindachnerina insculpta (Fernandez-Yepez, 1948) (n = 18) and Triportheus nematurus (Kner, 1858) (n = 5).

The presence of metacercariae of A. compactum was confirmed in five fish species in the Santa Barbara river: P. squamosissimus, S. nasutus, S. papaterra, H. malabaricus, and M. maculatus. Plagioscion squamosissimus (90%) and S. pappaterra (60%) presented the highest prevalence, mean intensity of infection and mean abundance (Table 1).

The metacercariae (Figure 2, Table 2) of A. compactum presented a foliaceous body, slightly concave in the ventral face and with a small conical segment in the posterior region; a small subterminal oral sucker, two lateral pseudosuckers in the anterior region; oval pharynx, short esophagus, intestinal caeca ending near the posterior region; oval holdfast (tribocytic organ). Gland cells occupying most of anterior region, extending from the beginning of intestinal caeca to the anterior region of the tribocytic organ and small gonads in the posterior region, after the tribocytic organ, were observed.

[FIGURE 2 OMITTED]

Discussion

Among the species found infected by A. compactum in the present study, P. squamosissimus, S. pappaterra and H. malabaricus had previously been recorded as hosts for this digenetic metacercariae (PAVANELLI et al., 2000; MACHADO et al., 2005; PAVANELLI et al., 2006). However, S. nasutus and M. maculatus are new hosts recorded for A. compactum metacercariae.

The morphological and morphometrical data of A. compactum metacercariae from Nova Avanhandava reservoir are in accordance with other morphological studies (Table 2) for this species (KOHN et al., 1995; SANTOS et al., 2002; NOVAES et al., 2006; ZICA et al., 2009).

It is emphasized that, in P. squamosissimus, parasitic levels were considerably higher. This species, from the Amazon Basin, was introduced by the Energy Company of Sao Paulo (CESP), in reservoirs under its responsibility from 1966 to 1973 (TORLONI et al., 1993). According to Pojmanska and Chabros (1993), the prevalence of diplostomid in introduced fish is higher when compared with that of indigenous fish. This finding was also observed by Machado et al. (2005), who found higher rates of infection in fish introduced into the floodplain of the upper Parana river, and P. squamosissimus species with the highest prevalence and intensity of infection. These authors suggest that probably A. compactum was introduced along with P. squamosissimus, which justified its higher prevalence and intensity of infection. However, native species may have been acting as intermediate hosts, to which the adaptation of metacercariae of A. compactum would thus justify the low prevalence rates and intensity of infection in these fish.

The introductions, depending on the fish species, can promote reductions of the native stocks or local extinctions, as result of several factors including dissemination of pathogens and parasites (AGOSTINHO; JULIO JUNIOR, 1996). The infection with A. compactum metacercariae in several fish species shows that the low specificity of the parasite favors its spread, infecting other species of native fish, and the parasite appears to have found appropriate ecological conditions for its parasite cycle (snails, fish and birds) in many aquatic ecosystems (MACHADO et al., 2005; RUIZ; AGUILAR, 2005).

In this reservoir, the elements necessary for the biological cycle of the parasite are present. Studies have demonstrated the occurrence of gastropod mollusks Biomphalaria sp. Preston, 1910 (FRANCA et al., 2007) and also birds of the genus Casmerodius Gloger, 1842 and Phalacrocorax Brisson, 1760. In this environment, H. malabaricus, M. maculatus, P. squamosissimus, S. pappaterra and S. nasutus serve as an intermediate host for A. compactum. However, we postulate that this helminth adapted better to P. squamosissimus and S. pappaterra, and that S. nasutus and M. maculatus are sporadical secondary intermediate hosts or even an accidental infection case, also suggesting a low specificity of this parasite.

DOI: 10.4025/actascibiolsci.v32i3.5675

Acknowledgements

The authors are grateful to the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico--CNPq (process no. 133203/2004-2 and 140838/2007-4), Fundacao de Amparo a Pesquisa do Estado de Sao Paulo--Fapesp (process no. 03/11239-2) and Fundacao para o Desenvolvimento da Unesp--Fundunesp (process no. 00329/04) support. This work complies with the current Brazilian laws.

Received on November 1, 2008.

Accepted on June 1, 2009.

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Jaciara Vanessa Kruger Paes *, Edmir Daniel Carvalho and Reinaldo Jose Silva

Instituto de Biociencias, Universidade Estadual Paulista "Julio de Mesquita Filho", Distrito de Rubiao Junior, s/n, 18618-970, Botucatu, Sao Paulo, Brazil. * Auhtor for correspondence. Email: jvkpaes@gmail.com
Table 1. Parasitism by Austrodiplostomum compactum in the eyes of
fish from the Nova Avanhandava reservoir, low Tiete river,
municipality of Buritama, Sao Paulo State, Brazil.

Fish species                       N   P (%)    MII       MA

Plagioscion squamosissimus (a)   213   90.1    20.8   18.718
Schizodon nasutus                 84    4.8     1.2    0.059
Satanoperca pappaterra (a)        25     60     6.4    3.840
Hoplias malabaricus                7   14.3       9    1.286
Metynnis maculatus (a)           298   0.33       1    0.003

N-number of collected fish; P-prevalence; MII-mean intensity
of infection; MA-mean abundance; (a) introduced species (AGOSTINHO
et al., 2007; LANGEANI et al., 2007).

Table 2. Morphometrical data of Austrodiplostomum compactum
(Diplostomidae) metacercariae.

                                    Kohn et          Santos et
                                  al. (1995)         al. (2002)

                                 Plagioscion        Plagioscion
Host                          squamosissimus     squamosissimus

Number of specimens                       14                 20
Length                      1470-2740 (2170)    880-1840 (1434)
Width                         600-1180 (970)      400-792 (611)
Length of conical segment         41-97 (77)                 --
Oral sucker
Length                            41-97 (77)         44-90 (65)
Width                            56-116 (79)         40-64 (52)
Lateral pseudosucker (1)
Length                                    --                 --
Width                                     --                 --
Lateral pseudosucker (2)
Length                                    --                 --
Width                                     --                 --
Prepharynx
Length                                    --           2-10 (6)
Width                                     --         10-24 (17)
Pharynx
Length                            64-94 (83)         50-64 (62)
Width                             45-79 (60)         40-60 (49)
Esophagus
Length                                    --                 --
Width                                     --                 --
Tribocytic organ
Length                         326-650 (507)      200-600 (285)
Width                          251-500 (370)      160-232 (182)

                                   Santos et           Novaes et
                                   al. (2002)          al. (2006)

                            Cicchla ocellaris           Geophagus
Host                                                 brasiliensis

Number of specimens                        20                   5
Length                        960-2480 (1462)    1584-1947 (1800)
Width                           560-960 (711)       537-706 (642)
Length of conical segment                  --                  --
Oral sucker
Length                             40-98 (68)          45-83 (59)
Width                              30-98 (56)          54-77 (68)
Lateral pseudosucker (1)
Length                                     --                  --
Width                                      --                  --
Lateral pseudosucker (2)
Length                                     --                  --
Width                                      --                  --
Prepharynx
Length                               4-20 (9)                  --
Width                              16-38 (23)                  --
Pharynx
Length                             44-98 (68)          53-73 (61)
Width                              38-78 (52)          50-64 (56)
Esophagus
Length                                     --                  --
Width                                      --                  --
Tribocytic organ
Length                          200-496 (308)       422-434 (428)
Width                           120-320 (180)       220-319 (258)

                                    Zica et
                                  al. (2009)       Present study

                                  Hypostomus         Plagioscion
Host                                  regani      squamosissimus

Number of specimens                       10                  21
Length                      1570-2281 (1988)    1301-2386 (1911)
Width                          543-864 (756)       482-854 (678)
Length of conical segment                 --                  --
Oral sucker
Length                            69-102(91)          51-87 (71)
Width                             75-99 (84)          51-92 (73)
Lateral pseudosucker (1)
Length                          93-148 (132)                  --
Width                           68-157 (118)                  --
Lateral pseudosucker (2)
Length                          78-168 (131)                  --
Width                           85-146 (119)                  --
Prepharynx
Length                                    --                  --
Width                                     --                  --
Pharynx
Length                            57-85 (73)          49-84 (69)
Width                             57-80 (64)          45-74 (58)
Esophagus
Length                          86-139 (111)         54-101 (72)
Width                                     --          29-53 (39)
Tribocytic organ
Length                         287-414 (373)       205-554 (401)
Width                          178-310 (243)       127-347 (246)

                            Total variation
                            for the species

                                         --
Host

Number of specimens                      --
Length                             880-2740
Width                              400-1180
Length of conical segment             41-97
Oral sucker
Length                               40-102
Width                                30-116
Lateral pseudosucker (1)
Length                               93-148
Width                                65-146
Lateral pseudosucker (2)
Length                               78-168
Width                                85-146
Prepharynx
Length                                 2-20
Width                                 10-38
Pharynx
Length                                44-98
Width                                 38-80
Esophagus
Length                               54-139
Width                                 29-53
Tribocytic organ
Length                              200-650
Width                               120-660
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