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Revista Brasileira de Parasitologia Veterinária

On-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.22 no.1 Jaboticabal Jan./Mar. 2013

https://doi.org/10.1590/S1984-29612013000100018 

Full Article

Sphincterodiplostomum musculosum (Digenea, Diplostomidae) infecting Steindachnerina insculpta(Characiformes, Curimatidae) in the Chavantes Reservoir, Southeastern Brazil

Sphincterodiplostomum musculosum (Digenea, Diplostomidae) infectando Steindachnerina insculpta(Characiformes, Curimatidae) no reservatório de Chavantes, Sudeste do Brasil

Aline Cristina Zago1  * 

Lidiane Franceschini1 

Igor Paiva Ramos1 

Érica de Oliveira Penha Zica1 

Alison Carlos Wunderlich1 

Edmir Daniel Carvalho3 

Reinaldo José da Silva4 

1Programa de Pós-graduação em Ciências Biológicas, Instituto de Biociências, Universidade Estadual Paulista – UNESP, Botucatu, SP, Brasil

2Centro de Ciências Biológicas e da Saúde, Colegiado de Ciências Biológicas, Universidade Estadual do Oeste do Paraná – UNIOESTE, Cascavel, PR, Brasil

3Departamento de Morfologia, Instituto de Biociências, Universidade Estadual Paulista – UNESP, Botucatu, SP, Brasil

4Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista – UNESP, Botucatu, SP, Brasil


ABSTRACT

This study aimed to report the infection bySphincterodiplostomum musculosum metacercariae inSteindachnerina insculpta from the Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. Thirty specimens of S. insculpta were collected and 29 were infected with S. musculosum metacercariae (prevalence = 96.67%) in the eyes and visceral cavity. The mean intensity of infection and abundance were 96.6 ± 29.41 (7-846) and 93.3 ± 28.6 (0-846), respectively. Positive correlation was observed between parasite abundance in the eyes and standard length (rs = 0.5, p = 0.005), total weight (rs = 0.649, p = 0.0001), and condition factor (rs = 0.439, p = 0.0154). The high parasitism rates by S. musculosummetacercariae in S. insculpta can be an indicative that this fish species is highly susceptible to infection by this diplostomid, and even reflect the presence of a large abundance of the intermediate host. Moreover,S. musculosum metacercariae are reported for the first time in S. insculpta.

Key words: Diplostomid; metacercaria; Sphincterodiplostomum musculosum; Steindachnerina insculpta; condition factor; Paraná River basin

RESUMO

O presente estudo tem como objetivo relatar a infecção por metacercárias de Sphincterodiplostomum musculosum emSteindachnerina insculpta provenientes do Reservatório de Chavantes, médio Paranapanema, município de Ipaussu, Estado de São Paulo, Brasil. Foram coletados 30 espécimes de S. insculpta, sendo que 29 estavam infectados por metacercárias de S. musculosum (prevalência = 96,67%) nos olhos e na cavidade visceral. A intensidade média de infecção e abundância apresentaram valores de 96,6 ± 29,41 (7-846) e 93,3 ± 28,6 (0-846), respectivamente. Foi observada correlação positiva entre a abundância dos parasitas presentes nos olhos com relação ao comprimento padrão (rs = 0.5, p = 0.005), peso (rs = 0.649, p = 0.0001) e fator de condição (rs = 0.439, p = 0.0154). As altas taxas de parasitismo de metacercárias de S. musculosum em S. insculpta podem ser um indicativo de que esta espécie de peixe é altamente susceptível à infecção por este diplostomídeo, e até mesmo refletir a presença de grande oferta do hospedeiro intermediário. Além disso, este é o primeiro relato de parasitismo por metacercárias de S. musculosum emS. insculpta.

Palavras-Chave: Diplostomídeo; metacercária; Sphincterodiplostomum musculosum; Steindachnerina insculpta; fator de condição; bacia do rio Paraná

Introduction

Steindachnerina insculpta Fernández-Yépez, 1948 is a native fish from Brazil and its occurrence is restricted to the Paraná River basin. This fish species belongs to the family Curimatidae and is commonly known in Brazil as saguiru-do-rabo-amarelo (FROESE; PAULY, 2012).

Materials and Methods

Thirty specimens of S. insculpta were collected in January, 2009 in the Chavantes Reservoir (Figure 1), medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil (23° 7′ 36″ S and 49.59° 23′ 10″ W). Fish were collected using a nylon monofilament gillnet from 5:00 PM to 7:00 AM, totaling 14 hours of exposure. The fish specimens collected were transported to a laboratory where they were measured (cm), weighed (g) and necropsied. Organs and body cavities of S. insculpta were examined and the metacercariae found were collected, fixed in alcohol-formol-acetic acid solution under cover slip pressure. After that, they were stained with carmine according to Eiras et al. (2006).

Figure 1. Map of Brazil, highlighting the State of São Paulo and the sampling area at the Chavantes Reservoir, Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. 

Morphometric analysis of the metacercariae was accomplished using a computerized system for image analysis (Qwin Lite 3.1, Leica Microsystems, Wetzlar, Germany). All measurements were presented in micrometers and represented by the mean ± standard deviation (range). The ecological descriptors of parasitism (prevalence, abundance and mean intensity of infection) were calculated according to Bush et al. (1997). Spearman's rank correlation (rs) was used to study the correlations of the abundance of parasites present in the eyes in relation to standard length, total weight and condition factor - K (LE CREN, 1951). Statistical tests were performed using SigmaStat 3.1 (Systat Software Inc., California, USA), adopting a significance level of 5%.

Voucher specimens were deposited in the Coleção Helmintológica (CHIBB: 6972-6973), of the Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista – UNESP, municipality of Botucatu, State of São Paulo, Brazil.

Results

The mean standard length and total weight of the fish analyzed were 12.05 (9-16.5) cm and 39.95 (13.7-74.3) g, respectively.

Twenty-nine S. insculpta specimens were infected byS. musculosum metacercariae (prevalence = 96.67%). The larvae were found parasitizing the eyes (93.33%) and visceral cavity (10%). Two thousand seven hundred ninety-nine metacercariae were collected in the studied specimens, and the mean intensity of infection and abundance were 96.6 ± 29.41 (7-846) and 93.3 ± 28.6 (0-846), respectively.

A positive correlation was observed between parasite abundance and standard length (rs = 0.5, p = 0.005) (Figure 2), total weight (rs = 0.649, p = 0.0001) (Figure 3) and condition factor (rs = 0.439, p = 0.0154) (Figure 4).

Figure 2. Correlation between standard length and abundance ofSphincterodiplostomum musculosum from the Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. 

Figure 3. Correlation between total weight and abundance ofSphincterodiplostomum musculosum from the Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. 

Figure 4. Correlation between condition factor (K) and abundance ofSphincterodiplostomum musculosum from the Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. 

Description of S. musculosum metacercariae (based on 30 specimens) (Figure 5): body bipartite; forebody oval and concave ventrally; hindbody ovoid, much narrower and inserts sub-dorsally in the anterior segment. Forebody with three lobes: the median lobe is occupied by the oral sucker, and the pseudosuckers are located in the lateral lobes; circular tribocitic organ; acetabulum located below of the middle of the forebody; anterior testis asymmetrical and lateral; posterior testis larger than the anterior one, consisting of two elongated lateral masses; anterior ovary adjacent to the anterior testis; sub-terminal sphincter. The morphometric data ofS. musculosum metacercariae is summarized in Table 1.

Figure 5. Sphincterodiplostomum musculosum metacercariae found inSteindachnerina insculpta from the Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. a) total body; b) anterior testis (AT), posterior testis (PT), ovary (OV), sphincter (SP); c) acetabulum (AC), tribocitic organ (TO); d) oral sucker (OS), pseudosucker (PS), pharynx (PH). 

Table 1. Comparative morphometric data between Sphincterodiplostomum musculosum metacercariae of the Chavantes Reservoir, Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil, and Steindachnerina brevipinna from the tributaries Guairacá and Corvo of the low Paranapanema River, State of Paraná, Brazil, described by Ceschini et al. (2010a)

Data and measures (µm) ofSphincterodiplostomum musculosummetacercariae Host
Steindachnerina insculptaa Steindachnerina brevipinnab
Mean ± SD (range) Mean (range)
Locality Chavantes Reservoir, medium Paranapanema River, State of São Paulo, Brazil Tributaries Guairacá and Corvo of the low Paranapanema River, State of Paraná, Brazil
Number of metacercariae 30 15
Body
Length 2734 ± 508.8 (2151-3982) 2553 (1775-3075)
Width 1272.4 ± 231 (914.4-1844.3) 1396 (1075-1675)
Anterior segment
Length 1642.6 ± 330.9 (1133.9-2346.9) 1530 (1150-1900)
Width 1272.4 ± 230.9 (914.4-1844.3) 1508 (1075-1675)
Posterior segment
Length 1087.4 ± 259.9 (810.9-1811.1) 1033 (600-1375)
Width 572.8 ± 79.4 (452.8-745.4) 665 (500-800)
Pharynx
Length 114.8 ± 27.5 (89.6-218.5) 104 (84-117)
Width 73.1 ± 16.1 (47.9-113.4) 54 (45-84)
Oral sucker
Length 142 .4 ± 34.5 (96.3-292.6) 145 (100-200)
Width 180.5 ± 31.5 (134.8-313.6) 213 (130-200)
Lateral pseudosucker (1)
Length 216.4 ± 57.7 (161.5-475.9) -
Width 261.1 ± 46.2 (186.8-438.4) -
Lateral pseudosucker (2)
Length 217.9 ± 56.6 (1149.8-461.4) -
Width 252.8 ± 50.4 (168.3-454.5) -
Ventral sucker
Length 142.4 ± 34.5 (96.3-292.6) 162 (130-210)
Width 180.5 ± 31.5 (134.8-313.6) 213 (180-250)
Tribocitic organ
Length 391.5 ± 85.1 (246-644.6) 384 (290-440)
Width 494.9 ± 107.2 (321.2-732.4) 490 (350-650)
Anterior testis
Length 285.4 ± 62.2 (199.8-452.7) 217 (130-390)
Width 293.2 ± 49.8 (209.4-414.3) 307 (250-350)
Posterior testis
Length 310.1 ± 58.9 (210-446.6) 290 (210-400)
Width 385.1 ± 79.6 (275.2-557.9) 410 (200-510)

aPresent study (CHIBB: 6972-6973);

b Ceschini et al. (2010a); Range = min-max; SD = standard deviation (mean).

Taxonomic Summary

Host: Steindachnerina insculptaFernández-Yépez, 1948.

Site of infection: eyes and visceral cavity.

Locality: Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil.

Material: CHIBB (6972-6973)

Mean Intensity of infection: 96.6 ± 29.41, up to 846 parasites found in a single host.

Prevalence: 96.67%.

Others hosts: Steindachnerina brevipinna Eigenmann and Eigenmann, 1889 (CESCHINI et al., 2010a), Hoplias malabaricus Bloch, 1794, (TAKEMOTO et al., 2009) and Cyphocharax gilbert Quoy and Gaimard, 1824 (ABDALLAH et al., 2005) to Sphincterodiplostomum musculosumDubois, 1936 metacercariae; and Hemisorubim platyrhynchosValenciennes, 1840 (TAKEMOTO et al., 2009) and Prochilodus lineatus Valenciennes, 1836 (LIZAMA et al., 2006) to Sphincterodiplostomumsp. Dubois, 1936 metacercariae.

Discussion

The present study reports the infection by S. musculosummetacercariae in S. insculpta from the Chavantes Reservoir, medium Paranapanema River, municipality of Ipaussu, State of São Paulo, Brazil. This parasite species was reported in a few fish species (CESCHINI et al., 2010a; TAKEMOTO et al., 2009; ABDALLAH et al., 2005) in comparison with other diplostomidae, such as Austrodiplostomum compactum, which was previously reported in approximately 25 fish species (MACHADO et al., 2005; EIRAS et al., 2010; PAES et al., 2010). Furthermore, the studied S. insculpta specimens presented high parasitism rates of S. musculosum, indicating that this fish species is high susceptible to infection by this parasite.

The morphological and morphometric data observed in this study toS. musculosum metacercariae from S. insculptacorroborated the data presented by Ceschini et al. (2010a), who found a high quantity of this diplostomid in the ovaries of S. brevipinna.

The abundance of S. musculosum in the eyes of S. insculpta was positively correlated to the standard length and total weight. Similar results were found by Ceschini et al. (2010b), who observed positive correlation between the abundance of S. musculosum and the standard length of S. brevipinna from the tributaries Guairacá and Corvo, in the low Paranapanema River, State of Paraná, Brazil. According to Ceschini et al. (2010b), these results support the idea of cumulative effect of parasites by increasing the area of infection with the growth of the host, as mentioned by Luque et al. (1996), and with the increase of the standard length with the ontogenetic development of the host, the area of the body surface also increases, as well as the possibility of occurring the process of active penetration of cercariae. This pattern was also observed by Paes et al. (2010) and Machado et al. (2005) in relation to other diplostomidae, such asAustrodiplostomum compactum metacercariae.

Positive correlation was also observed between the condition factor (K) and the abundance of S. musculosum in the eyes ofS. insculpta. The condition factor is given by the relationship between the individual's weight and length and it is an important indicator of the fish health, reflecting recent nutritional conditions and the interactions between the fish and the biotic and abiotic factors (LE CREN, 1951; SATAKE et al., 2009). Thus, the results observed in this study suggest that the parasitism by S. musculosumcould not affect the physiological status, health or welfare of the studiedS. insculpta specimens.

Sphincterodiplostomum musculosum found in this study were in the larval stage, suggesting that this fish species occupies an intermediate position in the food chain and may be part of the diet of piscivorous birds (definitive hosts of this parasite species).

In this study, a great number of S. musculosummetacercariae was found parasitizing the eyes of S. insculpta. According to Evans et al. (1976), around 40 metacercariae of diplostomids per eye may be responsible for cataract or blindness in fish (depending on the size of the host). In our study, no histopathological study was performed to analyze whether the S. insculpta specimens were affected by the parasites. However, the fact that the metacercariae were found parasitizing the eyes at high infection rates makes the fish an easier prey for capture by the definitive host (commonly piscivorous birds), so the parasite can complete its life cycle faster (ABDALLAH et al., 2005).

In summary, the high parasitism rates by S. musculosummetacercariae in S. insculpta can be an indicative that this fish species is highly susceptible to infection by this diplostomid, and even reflect the presence of a large abundance of the intermediate host. Moreover, S. musculosum metacercariae are reported for the first time in S. insculpta.

Acknowledgements

The authors are grateful to the Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) for the financial support (Process 2007∕58246-4 and 2008∕58792-1).

References

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Received: July 8, 2012; Accepted: November 26, 2012

*Corresponding author: Aline Cristina Zago, Instituto de Biociências, Universidade Estadual Paulista – UNESP, Distrito de Rubião Junior, CEP 18618-970, Botucatu, SP, Brasil, e-mail:alinecristhina@yahoo.com.br

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