New host records and a checklist of fishes infected with Austrodiplostomum compactum (Digenea: Diplostomidae) in Brazil

Novos registros de hospedeiros e “checklist” de peixes infectados por Austrodiplostomum compactum (Digenea: Diplostomidae) no Brasil

Igor Paiva Ramos Lidiane Franceschini Aline Cristina Zago Érica de Oliveira Penha Zica Alison Carlos Wunderlich Edmir Daniel Carvalho Reinaldo José da Silva About the authors

Abstracts

This study reports the infection of fishes by Austrodiplostomum compactum metacercariae in the Chavantes reservoir, medium Paranapanema River, municipality of Ipaussu, São Paulo State, Brazil. Twenty-three fish species were analysed, and 13 were infected with A. compactum metacercariae (56.5%) in their eyes. The following six fish species are new hosts for this metacercaria: Crenicichla haroldoi (1/1), Eigenmannia trilineata (11/6), Hoplosternum littorale (11/1), Iheringichthys labrosus (17/2), Leporinus amblyrhynchus (11/1), and Piaractus mesopotamicus (3/1). These new species increase the number of Brazilian fish species infected with this parasite to 36. Based on these findings, we hypothesise that the metacercariae larval stage of the parasite has a low specificity for the second intermediate host (fish). The majority of fish species infected in Brazil belong to the Loricariidae and Cichlidae families. For the fish species with higher mean abundances in Brazil, six are non-native species, and currently, Plagioscion squamosissimus has the highest mean abundance. The majority of fish species infected with A. compactum in Brazil are concentrated in the Paraná basin, although this may be related to the distribution of researchers.

Freshwater fishes; parasite; Trematoda; metacercariae; infection; Paraná basin


Este estudo relata a infecção por metacercárias de Austrodiplostomum compactum em peixes do reservatório de Chavantes, médio Paranapanema, Ipaussu, São Paulo, Brasil. Vinte e três espécies de peixes foram analisadas, e 13 estavam infectadas com metacercárias (56,5%) em seus olhos. Seis espécies de peixes foram registradas como novos hospedeiros: Crenicichla haroldoi (1/1), Eigenmannia trilineata (11/6), Hoplosternum littorale (11/1), Iheringichthys labrosus (17/2), Leporinus amblyrhynchus (11/1), and Piaractus mesopotamicus (3/1), aumentando para 36 o número de peixes brasileiros infectados por este parasita. Assim, inferimos que este estágio larval do parasita possui baixa especificidade parasitária em relação ao seu segundo hospedeiro intermediário (peixes). No Brasil, a maioria das espécies de peixes infectadas pertence às famílias Loricariidae e Cichlidae. Quanto às espécies de peixes com as maiores abundâncias médias no Brasil, seis são espécies não-nativas, sendo Plagioscion squamosissimus a espécie com a maior abundância média. Ainda, a maioria das espécies de peixes infectadas por A. compactum no Brasil, estão concentradas na bacia do Paraná, sendo este fato possivelmente relacionado com a distribuição de pesquisadores.

Peixes de água doce; parasita; Trematoda; metacercária; infecção; bacia do Paraná


Introduction

Eye fluke diplostomids have complex life cycles, involving three hosts, of which two are intermediate and one is definitive (KARVONEN et al., 2006Karvonen A, Savolainen M, Seppälä O, Valtonen ET. Dynamics of Diplostomum spathaceum infection in snail hosts at a fish farm. Parasitol Res 2006; 99(4): 341-345. http://dx.doi.org/10.1007/s00436-006-0137-8
http://dx.doi.org/10.1007/s00436-006-013...
; VIOLANTE-GONZáLEZ et al., 2009Violante-González J, García-Varela M, Rojas-Herrera A, Guerrero SG. Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, Mexico. Parasitol Res 2009; 105(3): 803-807. http://dx.doi.org/10.1007/s00436-009-1458-1
http://dx.doi.org/10.1007/s00436-009-145...
), and parasitise several fish species in the world (EIRAS, 1994Eiras JC. Elementos de ictioparasitologia. Porto: Fundação Engenheiro Antônio de Almeida; 1994.). Austrodiplostomum compactum (Lutz, 1928) is widely distributed in the Neotropical region, and A. compactum metacercaria parasitise several species of Brazilian freshwater fishes.

The A. compactum cercariae (first larval stage) infect aquatic snails and molluscs of the genus Biomphalaria Preston, 1910 in Mexico (VIOLANTE-GONZáLEZ et al., 2009Violante-González J, García-Varela M, Rojas-Herrera A, Guerrero SG. Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, Mexico. Parasitol Res 2009; 105(3): 803-807. http://dx.doi.org/10.1007/s00436-009-1458-1
http://dx.doi.org/10.1007/s00436-009-145...
) and Brazil (PINTO; MELO, 2013Pinto HA, Melo AL. Biomphalaria straminea and Biomphalaria glabrata (Mollusca: Planorbidae) as new intermediate hosts of the fish eyefluke Austrodiplostomum compactum (Trematoda: Diplostomidae) in Brazil. J Parasitol 2013; 99(4): 729-733. http://dx.doi.org/10.1645/12-13.1
http://dx.doi.org/10.1645/12-13.1...
). Diplostomum and Austrodiplostomum metacercariae are frequently found in the eyes of freshwater fishes, which are the second intermediate hosts during the life cycle of the parasite (SEPPÄLÄ et al., 2004Seppälä O, Karvonen A, Valtonen ET. Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Anim Behav 2004; 68(2): 257-263. http://dx.doi.org/10.1016/j.anbehav.2003.10.021
http://dx.doi.org/10.1016/j.anbehav.2003...
). The adult stage parasitises the digestive tract of piscivorous birds, and Phalacrocorax brasilianus (Gmelin, 1789) [=Phalacrocorax olivaceus] is considered definitive host of this digenean in Brazil (TRAVASSOS et al., 1969; NORONHA et al., 2009Noronha D, Sá MR, Knoff M, Muniz-Pereira LC, Pinto RM. Adolpho Lutz e a coleção helmintológica do Instituto Oswaldo Cruz. Rio de Janeiro: Museu Nacional; 2009.; MONTEIRO et al., 2011Monteiro CM, Amato JFR, Amato SB. Helminth parasitism in the Neotropical cormorant, Phalacrocorax brasilianus, in Southern Brazil: effect of host size, weight, sex, and maturity state. Parasitol Res 2011; 109(3): 849-855. http://dx.doi.org/10.1007/s00436-011-2311-x
http://dx.doi.org/10.1007/s00436-011-231...
).

According to Eiras (1994)Eiras JC. Elementos de ictioparasitologia. Porto: Fundação Engenheiro Antônio de Almeida; 1994. and Seppälä et al. (2005)Seppälä O, Karvonen A, Valtonen ET. Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Anim Behav 2005; 70(4): 889-894. http://dx.doi.org/10.1016/j.anbehav.2005.01.020
http://dx.doi.org/10.1016/j.anbehav.2005...
, the presence of Diplostomidae metacercariae in eyes of fishes can cause loss of vision, blindness and increases the coverage of cataracts of the lens area in fish with high rates of infection. This makes the fish more susceptible to predation and facilitates the transmission of the parasite to the definitive hosts (SEPPÄLÄ et al., 2004Seppälä O, Karvonen A, Valtonen ET. Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Anim Behav 2004; 68(2): 257-263. http://dx.doi.org/10.1016/j.anbehav.2003.10.021
http://dx.doi.org/10.1016/j.anbehav.2003...
).

However, a few Brazilian fish species were evaluated for the presence of A. compactum metacercariae and their possible effects. This study reports the occurrence of A. compactum in fish species from the Paranapanema River and its parasitological indexes, as well as several considerations regarding ecological aspects and a checklist for fishes parasitised in Brazil.

Materials and Methods

This study was conducted in the Chavantes reservoir (medium Paranapanema River), municipality of Ipaussu, São Paulo State, Brazil (23° 07′ 36″ S and 49° 59.23′ 10″ W) (Figure 1 and Table 1). Fish samples were collected monthly from March 2009 to February 2010 using gillnets (3 to 14 cm meshes between adjacent nodes) with 14 hours of exposure (from 5:00 PM to 7:00 AM). All captured fishes were frozen and transported to the laboratory where their eyes were removed and examined with a stereomicroscope. The metacercariae were collected from the vitreous humour, fixed in 70% alcohol under cover slip pressure and preserved in 70% alcohol (EIRAS et al., 2006Eiras JC, Takemoto MR, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. 2nd ed. Maringá: EdUEM; 2006.). The metacercariae were stained with carmine and cleared with eugenol for identification. Morphological analyses were performed with a computerised system for image analysis (Qwin Lite 3.2 – Leica Microsystems, Wetzlar, Germany).

Figure 1.
Map of the hydrographical network in São Paulo State highlighting the Chavantes reservoir and sampling location on the Paranapanema River in the municipality of Ipaussu, São Paulo State, southeast Brazil.

Table 1.
Physical and chemical characteristics (mean and standard error) of the sampling sites in the Chavantes Reservoir, municipality of Ipaussu, São Paulo State, southeast Brazil from Carvalho et al. (2012a)Carvalho ED, Silva RJ, Ramos IP, Paes JVK, Zanatta AS, Brandão H, et al. Ecological Features of Large Neotropical Reservoirs and Its Relation to Health of Cage Reared Fish. In: Carvalho ED, David-Silva G, Silva RJ. Health and environment in aquaculture. Rijeka: InTech; 2012a. p. 361-382. http://dx.doi.org/10.5772/2462
http://dx.doi.org/10.5772/2462...
.

Twenty-three fish species were analysed: ‘peixe-cachorro’, Acestrorhynchus lacustris n=33 (Lütken, 1875), ‘canivete’, Apareiodon affinis n=41 (Steindachner, 1879), ‘lambari-do-rabo-amarelo’, Astyanax altiparanae n=37 Garutti & Britski, 2000, ‘lambari-do-rabo-vermelho’, Astyanax fasciatus n=30 (Cuvier, 1819), ‘saguiru-do-rabo-vermelho’, Cyphocharax modestus n=1 (Fernández-Yépez, 1948), ‘peixe-cadela’, Galeocharax knerii n=32 (Steindachner, 1879), ‘traíra’, Hoplias malabaricus n=9 (Bloch, 1794), ‘piava’, Leporinus amblyrhynchus n=11 Garavello & Britski, 1987, ‘ferreirinha’, Leporinus octofasciatus n=1 Steindachner, 1915, ‘pacu’, Piaractus mesopotamicus n=3 (Holmberg, 1887), ‘ximborê’, Schizodon nasutus n=17 Kner, 1858, ‘piranha’, Serrasalmus maculatus n=21 Kner, 1858, ‘sardela’, Triportheus nematurus n=6 (Kner, 1858), ‘caborja’, Hoplosternum littorale n=11 (Hancock, 1828), ‘cascudo’, Hypostomus regani n=4 (Ihering,1905), ‘mandiuva’, Iheringichthys labrosus n=17 (Lütken, 1874), ‘mandi-guaçu’, Pimelodus maculatus n=34 Lacépède, 1803, ‘bagre’, Rhamdia quelen n=1 (Quoy & Gaimard, 1824), ‘tucunaré’, Cichla kelberi n=42 Kullander & Ferreira, 2006, ‘joaninha’, Crenicichla haroldoi n=1 Luengo & Britski, 1974, ‘acará’, Geophagus brasiliensis n=2 (Quoy & Gaimard, 1824), ‘corvina’, Plagioscion squamosissimus n=30 (Heckel, 1840), and ‘tuvira’, Eigenmannia trilineata n=11 López & Castello, 1966.

The prevalence, mean intensity of infection and mean abundance were calculated according to Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227
http://dx.doi.org/10.2307/3284227...
for fish species with at least nine specimens collected. Parasite voucher specimens were deposited in the Coleção Helmintológica do Departamento de Parasitologia (CHIBB 6723, 6974-6985) at the Instituto de Biociências, Universidade Estadual Paulista (IB/UNESP), municipality of Botucatu, São Paulo State, Brazil. Fish voucher specimens were identified and deposited by Dr. Cláudio de Oliveira in the Coleção do Laboratório de Biologia e Genética de Peixes (LBP 4797, 9192, 9174, 9179, 9181, 9183, 9184, 9185, 9186, 9191, 9194) at IB/UNESP and the Coleção Ictiológica do Nupélia (NUP 6117), Universidade Estadual de Maringá, municipality of Maringá, Paraná State, Brazil.

A review of the fishes infected with A. compactum in Brazil was performed using books (EIRAS et al., 2010Eiras CJ, Takemoto MR, Pavanelli GC. Diversidade dos parasitas de peixes de água doce do Brasil. Maringá: Clichetec; 2010.) and by searching databases (SciELO, ISI, Scopus and Google Scholar). When available, data regarding the prevalence, mean intensity of infection and mean abundance along with their errors or standard deviations were added to the Table. In cases where these data do not exist but data does exist that enable their calculations, we performed the calculations according to the method described by Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227
http://dx.doi.org/10.2307/3284227...
.

Results

In the present study, the fish collected in the Paranapanema River showed a total of 357 A. compactum metacercariae, recovered from 43 fish specimens. Thirteen fish species were infected by at least one parasite (56.5% of the fish species analysed), C. kelberi, C. haroldoi, E. trilineata, G. brasiliensis, H. regani, H. littorale, H. malabaricus, I. labrosus, L. amblyrhynchus, P. mesopotamicus, P. maculatus, P. squamosissimus, and S. nasutus, of which, two were non-native species, C. kelberi and P. squamosissimus.

Of the thirteen species of fish parasitised (192 specimens), the prevalence was 22.3% (43 fishes). Six freshwater fish species were identified as new hosts for A. compactum metacercariae, C. haroldoi, E. trilineata, H. littorale, I. labrosus, L. amblyrhynchus, and P. mesopotamicus, totalling 46.2% of the infected fish species and 26.1% for all the fish species analysed. Three fish orders, Characiformes, Perciformes, and Siluriformes had four parasitised fish species, and Gymnotiformes had one infected fish species. The Cichlidae family had three infected species (23.1%), followed by Pimelodidae and Anostomidae, with two infected species each (15.4%) (Table 2).

Table 2.
List of fish species reported as an intermediate host of Austrodiplostomum compactum metacercariae in Brazil. Number of specimens examined (N), prevalence (P), mean intensity of infection (MII), mean abundance (MA) and site of infection (SI).

The overall prevalence was 10.9%, and the highest prevalence was observed in P. squamosissimus (66.6%), followed by E. trilineata (54.5%) and I. labrosus (11.8%). The mean intensity of infection and mean abundance were low for all fish species, with P. squamosissimus having the highest values (13.1±6.1 and 8.7±4.2, respectively). All other fish species had values less than or equal to 2.0 for the mean intensity of infection and less than 1.0 for the mean abundance (Table 2).

Austrodiplostomum compactum metacercariae parasitised 36 Brazilian fish species and two taxa not identified (Cichla sp. and Hypostomus sp.) belonging to 13 families and four orders. The reports identified the fish species as follows: Characiformes (families: Anostomidae, three species; Curimatidae, one species; Erythrinidae, one species; and Serrasalmidae, four species); Siluriformes (families: Auchenipteridae, two species; Callichthyidae, one species; Loricariidae, eight species; and Pimelodidae, three species); Gymnotiformes (families: Gymnotidae, one species; and Sternopygidae, one species); and Perciformes (families: Centropomidae, one species; Cichlidae, 10 species; and Sciaenidae, one species). Eight infected fish species are non-native according to Langeani et al. (2007)Langeani F, Corrêa e Castro RM, Oyakawa OT, Shibatta OA, Pavanelli CS, Casatti L. Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotrop 2007; 7(3): 181-197.: Cichla sp., C. kelberi, C. ocellaris, G. proximus, G. surinamensis, Metynnis maculatus, P. squamosissimus and Satanoperca pappaterra (Table 2).

Of the 36 fish species parasitised, only eight showed a mean abundance higher than five metacercariae. Of these fishes, six are non-native species of the order Perciformes. The non-native species, P. squamosissimus had the highest mean abundance of all the parasitised species (Table 2). The Paranapanema River showed the highest number of parasitised fish species (21), followed by the Paraná River (nine species), Tietê and Guandu Rivers (seven species each) and Grande River (two species). The other rivers had one fish infected species each (Table 2).

Discussion

Austrodiplostomum compactum metacercariae have been recorded in a wide variety of Brazilian fishes (Table 2). This study demonstrated that 56.5% of all fish species collected were infected. These fish species belong to four orders, Characiformes, Perciformes, Siluriformes and Gymnotiformes, and six new records of hosts to these metacercariae. Thus, the number of Brazilian fish species infected by A. compactum increased to 36, and the number of families parasitised for 13. Based on these observations, we hypothesise that this larval stage of the parasite has a low specificity for the second intermediate host (fish), similar to that reported by Yamada et al. (2008)Yamada FH, Moreira LHA, Ceschini TL, Takemoto RM, Pavanelli GC. Novas ocorrências de metacercária de Austrodiplostomum compactum (Lutz, 1928) (Platyhelminthes: Digenea) parasito de olhos de peixes da bacia do rio Paraná. Rev Bras Parasitol Vet 2008; 17(3): 163-166. http://dx.doi.org/10.1590/S1984-29612008000300010
http://dx.doi.org/10.1590/S1984-29612008...
. In addition, the six new hosts identified in the present study demonstrates that parasitological studies with fish communities should significantly expand the list of fish identified as second intermediate hosts for A. compactum.

The mean intensity of infection for the analysed fish species was lower than Höglund and Thulin (1990)Höglund J, Thulin J. The epidemiology of the metacercariae of Diplostomum baeri and D. spathaceum in perch (Perca fluviatilis) from the warm water effluent of a nuclear power station. J Helminthol 1990; 64(2): 139-150. PMid:2387975. http://dx.doi.org/10.1017/S0022149X00012050
http://dx.doi.org/10.1017/S0022149X00012...
, who reports that fish harbouring more than 40 Diplostomum metacercariae on their eyes are largely parasitized. According to several authors, the high infection rate with diplostomid metacercariae in fish can cause blindness or visual impairment (EIRAS, 1994Eiras JC. Elementos de ictioparasitologia. Porto: Fundação Engenheiro Antônio de Almeida; 1994.), cataracts (SHARIFF et al., 1980Shariff M, Richards RH, Sommerville C. The histopathology of acute and chronic infections of rainbow trout Salmo gairdneri Richardson with eye flukes, Diplostomum spp. J Fish Dis 1980; 3(6): 455-465. http://dx.doi.org/10.1111/j.1365-2761.1980.tb00432.x
http://dx.doi.org/10.1111/j.1365-2761.19...
; KARVONEN et al., 2004), problems with a food intake and growth (OWEN et al., 1993Owen SF, Barber I, Hart PJB. Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 1993; 42(5): 803-806. http://dx.doi.org/10.1111/j.1095-8649.1993.tb00387.x
http://dx.doi.org/10.1111/j.1095-8649.19...
) and increased susceptibility to predation (CROWDEN; BROOM, 1980Crowden AE, Broom DM. Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav 1980; 28(1): 287-294. http://dx.doi.org/10.1016/S0003-3472(80)80031-5
http://dx.doi.org/10.1016/S0003-3472(80)...
; SEPPÄLÄ et al., 2004Seppälä O, Karvonen A, Valtonen ET. Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Anim Behav 2004; 68(2): 257-263. http://dx.doi.org/10.1016/j.anbehav.2003.10.021
http://dx.doi.org/10.1016/j.anbehav.2003...
). However, Karvonen et al. (2004) and Owen et al. (1993)Owen SF, Barber I, Hart PJB. Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 1993; 42(5): 803-806. http://dx.doi.org/10.1111/j.1095-8649.1993.tb00387.x
http://dx.doi.org/10.1111/j.1095-8649.19...
report effects in fish with less than 10 Diplostomum spathaceum metacercariae (Rudolphi, 1819) and correlations between the number of metacercariae and the intensity of the effect. Another study reported that fish heavily infected with D. spathaceum occupied surface waters with more frequency, exposing them to higher levels of predation by birds. Therefore, fish with high infection rates would be subject to the effects of parasitism by A. compactum metacercariae, and fish with low infection show less intense effects of parasitism. Among these effects is the difficulty to detect prey, which results in fitness consequences for the individual (OWEN et al., 1993Owen SF, Barber I, Hart PJB. Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 1993; 42(5): 803-806. http://dx.doi.org/10.1111/j.1095-8649.1993.tb00387.x
http://dx.doi.org/10.1111/j.1095-8649.19...
).

The prevalence of A. compactum in the present study is low, with exception of the prevalence in E. trilineata and P. squamosissimus. Studies of the infection of A. compactum in P. squamosissimus showed a prevalence greater than 90% and a mean intensity of infection greater than 20 (KOHN et al., 1995Kohn A, Fernandes BMM, Baptista-Farias MFD. Metacercariae of Diplostomum (Austrodiplostomum) compactum (Trematoda, Diplostomidae) in the eyes of Plagioscion squamosissimus (Teleostei, Sciaenidae) from the reservoir of the Hydroelectric Power Station of Itaipu, Brazil. Mem Inst Oswaldo Cruz 1995; 90(3): 341-344. http://dx.doi.org/10.1590/S0074-02761995000300005
http://dx.doi.org/10.1590/S0074-02761995...
; SANTOS et al., 2002Santos RS, Pimenta FDA, Martins ML, Takahashi HK, Marengoni NG. Metacercárias de Diplostomum (Austrodiplostomum) compactum Lutz, 1928 (Digenea: Diplostomidae) em peixes do rio Paraná, Brasil. Prevalência, sazonalidade e intensidade de infecção. Acta Sci Biol Sci 2002; 24(2): 475-480., 2012Santos RS, Marchiori N, Santarem VA, Takahashi K, Mourino JLP, Martins ML. Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) in the eyes of fishes from Paraná River, Brazil. Acta Sci Biol Sci 2012; 34(2): 225-231. http://dx.doi.org/10.4025/actascibiolsci.v34i2.9337
http://dx.doi.org/10.4025/actascibiolsci...
; MACHADO et al., 2005Machado PM, Takemoto RM, Pavanelli GC. Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) (Platyhelminthes, Digenea) metacercariae in fish from the floodplain of the Upper Paraná River, Brazil. Parasitol Res 2005; 97(6): 436-444. http://dx.doi.org/10.1007/s00436-005-1483-7
http://dx.doi.org/10.1007/s00436-005-148...
; PAES et al., 2010aPaes JVK, Carvalho ED, Silva RJ. Infection by Austrodiplostomum compactum metacercariae in fish from the Nova Avanhandava Reservoir, Tietê River, São Paulo, Brazil. Acta Sci 2010a; 32(3): 273-278. http://dx.doi.org/10.4025/actascibiolsci.v32i3.5675
http://dx.doi.org/10.4025/actascibiolsci...
, bPaes JVK, Carvalho ED, Silva RJ. Infection levels of Austrodiplostomum compactum (Digenea, Diplostomidae) metacercariae in Plagioscion squamosissimus (Teleostei, Sciaenidae) from the Nova Avanhandava reservoir, São Paulo State, Brazil. J Helminthol 2010b; 84(3): 284-291. PMid:19889255. http://dx.doi.org/10.1017/S0022149X09990617
http://dx.doi.org/10.1017/S0022149X09990...
), whereas in the current study, the prevalence was 66.6% and the mean intensity of infection was 13.1±6.1. According to Karvonen et al. (2006)Karvonen A, Savolainen M, Seppälä O, Valtonen ET. Dynamics of Diplostomum spathaceum infection in snail hosts at a fish farm. Parasitol Res 2006; 99(4): 341-345. http://dx.doi.org/10.1007/s00436-006-0137-8
http://dx.doi.org/10.1007/s00436-006-013...
, the infection dynamics of D. spathaceum in fish is related to the snail population variance. Voutilainen et al. (2009)Voutilainen A, Van Ooik T, Puurtinen M, Kortet R, Taskinen J. Relationship between prevalence of trematode parasite Diplostomum sp. and population density of its snail host Lymnaea stagnalis in lakes and ponds in Finland. Aquat Ecol 2009; 43(2) 351-357. http://dx.doi.org/10.1007/s10452-008-9203-x
http://dx.doi.org/10.1007/s10452-008-920...
found a positive correlation between Lymnaea stagnalis (Linnaeus, 1758) density (an intermediate host for Diplostomum spp. in Finland) and Diplostomum sp. prevalence in lakes and ponds in Finland. Additionally, Martins et al. (2002)Martins ML, Paiva AMFC, Fujimoto RY, Schalch SHC, Colombano NC. Prevalência, sazonalidade e intensidade de infecção por Diplostomum (Austrodiplostomum) compactum Lutz, 1928 (Digenea, Diplostomidae), em peixes do reservatório de Volta Grande, Estado de Minas Gerais, Brasil. Acta Sci Biol Sci 2002; 24(2): 469-474. and Santos et al. (2002Santos RS, Pimenta FDA, Martins ML, Takahashi HK, Marengoni NG. Metacercárias de Diplostomum (Austrodiplostomum) compactum Lutz, 1928 (Digenea: Diplostomidae) em peixes do rio Paraná, Brasil. Prevalência, sazonalidade e intensidade de infecção. Acta Sci Biol Sci 2002; 24(2): 475-480., 2012)Santos RS, Marchiori N, Santarem VA, Takahashi K, Mourino JLP, Martins ML. Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) in the eyes of fishes from Paraná River, Brazil. Acta Sci Biol Sci 2012; 34(2): 225-231. http://dx.doi.org/10.4025/actascibiolsci.v34i2.9337
http://dx.doi.org/10.4025/actascibiolsci...
suggested that high infection rates of A. compactum are dependent on high temperatures. According to Berrie (1960)Berrie AD. Two Diplostomulum larvae (Strigeida, Trematoda) in the eyes of sticklebacks (Gasterosteus aculeatus L.). J Helminthol 1960; 34(3-4): 211-216. http://dx.doi.org/10.1017/S0022149X00021143
http://dx.doi.org/10.1017/S0022149X00021...
, Diplostomum cercariae emerge in waters only at temperatures greater than 10 °C. Despite the high water temperature observed in the current study location (CARVALHO et al., 2012aCarvalho ED, Silva RJ, Ramos IP, Paes JVK, Zanatta AS, Brandão H, et al. Ecological Features of Large Neotropical Reservoirs and Its Relation to Health of Cage Reared Fish. In: Carvalho ED, David-Silva G, Silva RJ. Health and environment in aquaculture. Rijeka: InTech; 2012a. p. 361-382. http://dx.doi.org/10.5772/2462
http://dx.doi.org/10.5772/2462...
), which may lead to a high intensity of infection, the values of water transparency, conductivity and chlorophyll a (Table 1), suggest a small quantity of available nutrients in the local aquatic ecosystem. This can limit the size of the snail populations (first intermediate hosts), leading to the low values observed for the prevalence, mean intensity of infection and mean abundance for the majority fish species analysed.

The majority of fish species infected with A. compactum metacercariae in Brazil belong to the Perciformes (12 species), Siluriformes (13 species), and Characiformes (nine species), and the Cichlidae (10 species) and Loricariidae (eight species) families were the most infected. However, the other fish species analysed in this study also live in this habitat and were not infected. Therefore, the absence of A. compactum metacercariae infection in these fish species may be related to species-specific characteristics, which remain unknown.

For the fish species with higher mean abundances in Brazil, six are non-native species, and currently, P. squamosissimus has the highest mean abundance. This was also demonstrated by Pojmanska and Chabros (1993)Pojmanska T, Chabros M. Parasites of common carp and three introduced cyprinid fish in pond culture. Acta Parasitol 1993; 38(3): 101-108., who showed that the prevalence of diplostomids was significantly lower in native fishes than non-native fishes. However, Lacerda et al. (2012)Lacerda ACF, Takemoto RM, Tavares-Dias M, Poulin R, Pavanelli GC. Comparative parasitism of the fish Plagioscion squamosissimus in native and invaded river basins. J Parasitol 2012; 98(4): 713-717. http://dx.doi.org/10.1645/GE-2882.1
http://dx.doi.org/10.1645/GE-2882.1...
demonstrated an inverse situation in which the native fish H. malabaricus showed a higher abundance of Austrodiplostomum sp. than the introduced P. squamosissimus. Lacerda et al. (2012)Lacerda ACF, Takemoto RM, Tavares-Dias M, Poulin R, Pavanelli GC. Comparative parasitism of the fish Plagioscion squamosissimus in native and invaded river basins. J Parasitol 2012; 98(4): 713-717. http://dx.doi.org/10.1645/GE-2882.1
http://dx.doi.org/10.1645/GE-2882.1...
also demonstrated that P. squamosissimus in native regions showed a prevalence and abundance of diplostomids that was significantly lower than P. squamosissimus in the region where they were introduced. According to Lacerda et al. (2012)Lacerda ACF, Takemoto RM, Tavares-Dias M, Poulin R, Pavanelli GC. Comparative parasitism of the fish Plagioscion squamosissimus in native and invaded river basins. J Parasitol 2012; 98(4): 713-717. http://dx.doi.org/10.1645/GE-2882.1
http://dx.doi.org/10.1645/GE-2882.1...
, migratory birds, such as P. brasilianus are the final hosts for Austrodiplostomum; therefore, geographic barriers for the parasite may be reduced or eliminated. Rather than introducing a new parasite, P. squamosissimus may be acting as a new and suitable host for a local parasite. This may also occur with other species of fish, such as the six non-native Brazilian fish species, which had higher abundances.

The majority of infected fish species are in the Paranapanema River. Specifically, the Paraná basin is the most studied region for A. compactum in Brazil, and this is possibly related to the distribution of researchers in Brazil. Despite the large number of studies, further investigations are necessary to understand the relationship between environmental aspects and life strategies because diplostomiasis causes large aquaculture losses each year worldwide (PAPERNA; DZIKOWSKI, 1995Paperna I, Dzikowski R. Digenea (Phylum Platyhelminthes). In: Woo PT. Fish diseases and disorders. Vol. I: protozoans and metazoan infections. Wallingford: CAB International; 1995. p. 345-390.; OVERSTREET; CURRAN, 2004Overstreet R, Curran S. Defeating diplostomoid dangers in USA catfish aquaculture. Folia Parasitol 2004; 51(2-3): 153-165. PMid:15357393.).

The authors are grateful to the Instituto de Biociências de Botucatu (IBB) and Centro de Aquicultura (CAUNESP) – Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP, for the use of laboratory facilities and logistics. This study complies with current Brazilian laws. This study was supported by FINEP (Financiadora de Estudos e Pesquisas - process number: 3626/05) and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo - process number 2008/58792-1).

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  • Zica EOP, Brandão H, Zawadzki CH, Nobile AB, Carvalho ED, Silva RJ. The occurrence of Austrodiplostomum compactum (Lutz, 1928) (Digenea: Diplostomidae) metacercariae in the eyes of loricariid fish (Siluriformes: Osteichthyes: Loricariidae) from Brazil. J Helminthol 2011; 85(1): 73-79. http://dx.doi.org/10.1017/S0022149X10000271
    » http://dx.doi.org/10.1017/S0022149X10000271

Publication Dates

  • Publication in this collection
    Oct-Dec 2013

History

  • Received
    25 Apr 2013
  • Accepted
    1 Nov 2013
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