Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) in the eyes of fishes from Parana river, Brazil/Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) em olhos de peixes do rio Parana, Brasil.
Metacercariae of Diplostomum and Austrodiplostomum are frequently reported parasitizing freshwater fishes which are the second intermediate hosts in the parasite's life-cycle (RINTAMAKI-KINNUNEN et al., 2004; SEPPALA et al., 2004). Whereas the adult stage inhabits the digestive tract of piscivore birds, its larval cercariae stage may be found in aquatic mollusks. The parasite has a geographically wide range with reports from over 125 fish species (EIRAS, 1994).
There are several reports from Brazil on diplostomid metacercariae parasitizing fishes. Metacercariae have been found in Plagioscion squamosissimus Heckel, 1840 (KOHN et al., 1995; MACHADO et al., 2005; MARTINS et al., 2002; PAES et al., 2003, 2010; SANTOS et al., 2002; TAKEMOTO et al., 2009), Hypostomus regani Ihering, 1905 (TAKEMOTO et al., 2009; YAMADA et al., 2008; ZICA et al., 2009), Cichla monoculus Spix and Agassiz, 1831 (MACHADO et al., 2000, 2005; TAKEMOTO et al., 2009), Cichla ocellaris Bloch and Schneider, 1801 (MACHADO et al., 2005; SANTOS et al., 2002), Pimelodus maculatus Lacepede, 1803 (BRASIL-SATO; PAVANELLI, 2004; BACHMANN et al., 2007), Hoplias malabaricus Bloch, 1794 (MACHADO et al., 2005; TAKEMOTO et al., 2009), Satanoperca pappaterra Heckel, 1840 (MACHADO et al., 2005; TAKEMOTO et al., 2009), Geophagus brasiliensis Quoy and Gaimard, 1824 (AZEVEDO et al., 2006; NOVAES et al., 2006) and Crenicichla britskii Kullander, 1982 (MACHADO et al., 2005; TAKEMOTO et al., 2009), Serrasalmus maculatus Kner, 1858, Schizodon borellii Boulenger, 1900 and Auchenipterus osteomystax Mirando Ribeiro, 1918 (TAKEMOTO et al., 2009; YAMADA et al., 2008), Conorhynchos conirostris Valenciennes, 1840 (BRASIL-SATO; SANTOS, 2005), Cyphocharax Gilbert Quoy and Gaimard, 1824 (ABDALLAH et al., 2005) and Cichlasoma paranaense Kullander, 1983 (MACHADO et al., 2005; TAKEMOTO et al., 2009).
The River Parana is the second largest river in extension in South America and commercial fishing is one of its important local economic activities. Kohn et al. (1995), Santos et al. (2002), Brasil-Sato and Pavanelli (2004), Machado et al. (2005) and Yamada et al. (2008) have registered parasitosis by A. compactum in fishes from the Parana river basin.
Current research reports on the occurrence of Austrodiplostomum compactum (Lutz, 1928) in four fish species from the Parana river, as well as its ecological aspects with regard to parasitological indexes, rainfall and water quality.
Material and methods
Current research was undertaken at the Aquaculture Center of the Universidade do Oeste Paulista (UNOESTE), on the shores of the Parana river, near the town of Presidente Epitacio, state of Sao Paulo (21[degrees] 45' 48" S; 52[degrees] 06' 56" W). Fifty-one specimens of P. squamosissimus, 39 G. surinamensis, 27 H. malabaricus and 23 Cichla sp. were collected with gill nets and hooks, between June 2007 and June 2008, comprising
the winter of 2007 thru the winter of 2008, for parasitological exam undertaken according to Santos et al. (2002). Geophagus surinamensis, H. malabaricus and Cichla sp. were not captured during the summer of 2007. Parasite specimens were fixed in 5% formaldehyde, washed in distilled water, stained in carmine or diaphanized in beechwood creosote and mounted on permanent slides using Canada balsam. The terms prevalence, mean intensity of infection and mean parasite abundance were attributed according to Bush et al. (1997).
The water quality was monthly measured. Water temperature and dissolved oxygen were measured with digital oxymeter YSI 5512; ammonia, pH, and alkalinity were calculated with Merk's colorimetric method. Rainfall indexes were obtained from the meteorological station of the Universidade do Oeste Paulista (UNOESTE) in Presidente Prudente, Sao Paulo State, Brazil.
Collected data underwent statistical tests to compare rainfall, air temperature and water quality between seasons; to determine differences between the intensity of infection and abundance of parasites in fish between the seasons; to verify which fish species was more parasitized during the whole period and the possible differences in host weight and length for each fish species examined according to season. ANOVA and Bartlett's test for variance homogeneity were used, with significance for all statistical analyses set at [alpha] = 0.05.
Results and discussion
No significant differences in rainfall indexes between seasons were observed. However, temperature rates were high (p < 0.05) in the spring and summer 2007. The highest water temperatures (p < 0.05) occurred in the spring 2007, summer 2007 and autumn 2008. High alkalinity rates were reported in the winter and spring 2007 and autumn 2008, but no difference in pH and dissolved oxygen occurred during the seasons (Table 1).
Mean highest rainfall during the studied period occurred in the winter 2007, spring 2007 and autumn 2008. Oscillations occurred in water alkalinity and pH during the period under analysis. The highest temperature rates were registered between spring 2007 and autumn 2008, although there were considerable variations in all months. Dissolved oxygen levels also varied during the year (Table 1).
Metacercariae at different stages of development were collected from the crystalline of host's eyes in all fish species.
Except for autumn 2008, the prevalence of A. compactum in P. squamosissimus was 100%, even though the highest parasite numbers were observed in autumn 2008 (255) and spring 2007 (222) (Table 2). The mean highest infection intensities were reported in spring 2007 (45.0 [+ or -] 65.8) and in autumn 2008 (59.3 [+ or -] 70.0) (Table 2).
Parasites from G. surinamensis were reported only between autumn and winter 2008. Although no fish was collected in the summer 2008, mean infection intensities were low, varying between 12 and 18.2 parasites, and mean abundance varying between 10.4 and 18.2 (Table 3).
Prevalence of H. malabaricus varied from 46.6 to 83.3% between winter 2007 and autumn 2008 (Table 4). The highest number of parasites was registered in winter 2007 (247) with mean infection intensity (35.2 [+ or -] 18.2) and mean abundance (16.4), followed by winter 2008, with total number of parasites 214, mean intensity 71.3 [+ or -] 97.6 and abundance 53.5 (Table 4).
Metacercariae prevalence in Cichla sp. varied between 23 and 100%, with the mean lowest infection intensities (1.3 to 8.5 parasites). Therefore, mean abundance values varied from 0.3 to 7.1, with the highest number of parasites in the autumn 2008 (50) (Table 5).
Regardless of fish species, no significant difference (p > 0.05) between the seasons was reported in parasitological indexes. Contrastingly, when each fish species was analyzed regardless of the season, P. squamosissimus was found to be the most parasitized fish (p < 0.05).
No significant difference (p > 0.05) occurred between host weight and total length for all fish species between the seasons.
Santos et al. (2002) registered a positive relationship between mean infection intensity and rainfall, associated with high temperatures. Current study agrees with previous one in which all fish species were reported with the highest infection intensity during the months with the mean highest rainfall and which coincided with the highest temperatures.
In contrast, analyzing P. squamosissimus from Nova Avanhandava reservoir in the state of Sao Paulo, Brazil, Paes et al. (2010) did not report any influence either of aquatic parameters or of rainfall on the parasitic fauna. Since transmission is a major determinant of parasite fitness, perhaps other factors, such as local host population dynamics, fish feeding habits, strategies in cercarial release from first intermediate hosts and also the type of fresh water environments (lotic or lentic environment), would be primarily influencing success in parasite transmission.
There is a wide range of fish species collected from Brazil which are parasitized by metacercariae of A. compactum. Fifty percent of these fish species, namely, A. osteomystax, C. monoculus, C. ocellaris, S. pappaterra, H. malabaricus and P. squamosissimus, registered over 50% prevalence rates. The latter species achieved indexes up to 100% (Table 6). Plagioscion squamosissimus, also with mean high infection intensity, was the most parasitized fish species reported not only in current study but also in Santos et al. (2002), Martins et al. (2002) and Paes et al. (2010). Santos et al. (2002) reported the highest parasitological indexes in March 2001 for fish species, with infection intensities ranging from 4 to 137 parasites per host eye, while Martins et al. (2002) reported the highest infection intensities during late winter 2000 and late summer 2001. Although no significant difference in mean intensity and abundance of metacercariae throughout the seasons has been reported in current research, P. squamosissimus examined in spring and autumn had the highest parasitic load when compared to findings by Paes et al. (2010) in the same fish species in the Nova Avanhandava reservoir.
According to Lyholt and Buchmann (1996) and Hakalahti et al. (2006), infection of fishes by Diplostomum spathaceum (Rudolphi, 1819) metacercariae is temperature dependent. Hoglund and Thulin (1990) observed in their study that the maximum temperature (up to 23[degrees]C) coincided with the period of reduced recruitment of Diplostomum baeri Dubois 1937 metacercariae in perch Perca fluviatilis Linnaeus 1758. The highest prevalence and mean intensity observed in this study for P. squamosissimus, G. surinamensis and H. malabaricus were registered at water temperatures between 21.4 and 29.0[degrees]C. Such data may be explained by data from Hakalahti et al. (2006), according to whom extended summer temperatures would alter the dynamic population of cercariae and consequently the fish infection by metacercariae.
Due to the fact that water temperature at the collection site analyzed in current research was higher than that in Hakalahti et al. (2006), infection behavior at low temperatures cannot be evaluated. Martins et al. (2002) registered the positive influence of high temperatures on A. compactum infection in P. squamosissimus. In fact, their suggestion may be confirmed in current study for P. squamosissimus, a fish collected during the whole period under analysis. According to Berrie (1960), Diplostomum cercariae emerge in waters only at temperatures above 10[degrees]C. Lyholt and Buchmann (1996) registered that daily shedding of D. spathaceum cercariae in Lymnaea stagnalis (Linnaeus, 1758) reached a maximum of 58,000 cercariae [snail.sup.-1] [day.sup.-1] at 20[degrees]C and a maximum of 10,000 cercariae [snail.sup.-1] [day.sup.-1] at 10[degrees]C. These authors also concluded that cercariae were 4 to 5 times more infective at 15[degrees]C than at 7[degrees]C, reinforcing the impact of temperature on the parasite's life-cycle. Although adaptations in temperature margins would be expected to suit local conditions, it seems that parasite biology is dependent on high temperatures, as suggested by Santos et al. (2002), Martins et al. (2002) and Hakalahti et al. (2006).
Luque and Poulin (2004) compared 50 teleost fish species from the coast of Brazil to evaluate the effects of host traits on the richness and abundance of larval helminths and reported that among all the potential correlates, host body length was positively correlated with helminth larvae abundance. Machado et al. (2005) registered a positive correlation between C. britskii size and the prevalence of A. compactum and attributed this fact to the possibility of larger fish being easier targets for cercariae. The parasite load in P. squamosissimus increased with fish length, as reported by Paes et al. (2010). These authors also attributed the cumulative process to a greater body surface available for cercariae infection. According to Pojmanska (1994), there is evidence on the positive correlation between parasite number and fish size, arguing that accumulation is due to the metacercariae's long life. On the other hand, Valtonen and Gibson (1997) concluded that the diplostomid metacercariae infection in fishes from northern Finland provided little or no association between the prevalence of infection and host-size, even though there was a distinct accumulation in the number of parasites.
With regard to the above, Burrough (1978), analyzing the population biology of D. spathaceum in roach Rutilus rutilus and rudd Scardinius erythrophthalmus, concluded that parasite accumulation occurred up to the time fish reached 130 mm. Unfortunately, it was not possible to compare our results with those of the latter author due to the lack of analyzed fishes measuring less than 130 mm. This fact did not depend on fishing tactics since the animals were captured with hook and net, similar to that for collection species. No distinct accumulation was reported and thereafter intensity ranged between all levels.
The Brazilian records for diplostomid metacercariae parasitosis show different sites of parasite infection in the host's body, despite an apparent preference for the fish's eyes, including aqueous humor and crystalline (Table 6). Amato et al. (2001) recorded an unidentified Diplostomidae from kidney, body cavity, mesentery and brain of Loricariichthys anus (Valenciennes, 1835), whereas Brasil-Sato and Santos (2005) registered A. compactum (D. compactum) in the gills and eyes of C. conirostris (Table 6). According to Eiras (1994), reports by several authors suggest that Diplostomum species have their own location preferences. Bortz et al. (1988) verified that parasites collected from the hosts' retina and crystalline corresponded to populations with different epidemiological characteristics and thus different parasite species. Alternatively, the parasite infection site may be related to fish species. Whatever the mechanisms involved in parasite's preferences, more studies identifying correctly the parasite location and also a revision of the group systematics are necessary to elucidate this question. The taxonomy, especially regarding larval stages, is still unclear and several species, considered adults in nature, have never actually been observed as larvae and vice-versa (HOGLUND; THULIN, 1990).
Hoglund and Thulin (1990) state that fishes harboring more than 40 diplostomid metacercariae on their eyes are largely parasitized. In the present study, P. squamosissimus and H. malabaricus may therefore be considered the main host resources used by the parasite within the context of the river under analysis. It may be concluded that these fish species may not only be the most susceptible fish species but also good indicators of Austrodiplostomum infection.
The authors thank CNPq (National Council of Scientific and Technological Development) for Grant to M.L. Martins and CAPES (Coordination of Improvement of Higher Education Personnel) for scholarship to N.C. Marchiori.
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Received on February 4, 2010.
Accepted on June 30, 2010.
License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Rosemeire de Souza Santos (1), Natalia Marchiori (2), Vamilton Alvares Santarem (1), Haroldo Kazuyuki Takahashi (1), Jose Luis Pedreira Mourino (2) and Mauricio Laterca Martins (2) *
(1) Centro de Aquicultura, Universidade do Oeste Paulista, Presidente Prudente, Sao Paulo, Brazil. (2) Departamento de Aquicultura, Universidade Federal de Santa Catarina, Rod. Admar Gonzaga, 1346, 88040-900, Florianopolis, Santa Catarina, Brazil. * Author for correspondence. E-mail: email@example.com
Table 1. Rainfall, air temperature and water quality mean rates measured at the shores of the Parana river, near Presidente Epitacio, Sao Paulo State, Brazil. Rainfall Air temperature Water temperature Seasons (mm) ([degrees]C) ([degrees]C) Winter 2007 3.1 21.9 22.5 (0-90) (12.6-26.3) c (21.5-23.0) a Spring 2007 4.6 26.8 26.5 (0-54) (19.6-32.1) a (25.8-28.4) bc Summer 2007 2.1 27.7 29.0 c (0-28) (24.6-29.8) a Autumn 2008 5.7 23.7 25.7 (0-82) (16.2-28.4) b (26.2-27.3) b Winter 2008 0.8 20.6 21.4 (0-8) (13.0-24.8) c (21.3-21.6) a Alkalinity Oxygen Seasons (mg [L.sup.-1]) pH (mg [L.sup.-1]) Winter 2007 17.0 7.0 7.7 (15.0-18.0) ab (7.5-7.8) Spring 2007 18.7 7.0 6.9 (18.0-21.0) a (6.3-7.2) Summer 2007 15.0 a 6.8 5.6 Autumn 2008 16.9 7.0 6.3 (12.0-18.0) ab (6.8-8.0) (3.8-7.5) Winter 2008 13.8 7.0 7.7 (12.0-15.0) b (6.4-8.4) * Different letters indicate significant difference (p < 0.05) between the seasons. Table 2. Parasitological indexes ([+ or -] standard error) and biometry of Plagioscion squamosissimus parasitized by Austrodiplostomum compactum from the Parana river, region of Presidente Epitacio, Sao Paulo State, Brazil. Mean values and variation, between parentheses, of fish weight and length, infected fish/examined fish (IF/IE), prevalence, total number of parasites (TNP), mean intensity and range, between parenthesis, and mean abundance. Fish Fish Prevalence Seasons weight (g) length (cm) IF/EF (%) Winter 2007 480.1 33.3 16/16 100 (185-1360) (25-50) Spring 2007 626.0 33.8 15/15 100 (162-1998) (24-54) Summer 2007 497.0 32.8 6/6 100 (236-1290) (26.5-47) Autumn 2008 666.9 32.8 14/15 93.3 (214-2560) (25-52) Winter 2008 231.2 27.8 5/5 100 (166-276) (26-31) Seasons TNP Mean intensity Mean abundance Winter 2007 577 36.1 [+ or -] 7.2 36.1 [+ or -] 7.2 (2-90) Spring 2007 634 45.0 [+ or -] 20.8 45.0 [+ or -] 20.8 (7-222) Summer 2007 201 36.8 [+ or -] 14.4 36.8 [+ or -] 14.4 (12-92) Autumn 2008 831 59.3 [+ or -] 18.7 55.4 [+ or -] 17.9 (2-255) Winter 2008 148 29.6 29.6 [+ or -] 13.4 (1-76) Table 3. Parasitological indexes ([+ or -] standard error) and biometry of Geophagus surinamensis parasitized by Austrodiplostomum compactum from the Parana river, region of Presidente Epitacio, Sao Paulo State, Brazil. Mean values and variation, between parentheses, of fish weight and length, infected fish/examined fish (IF/IE), prevalence, total number of parasites (TNP), mean intensity and range, between parentheses, and mean abundance. Fish Fish Prevalence Seasons weight (g) length (cm) IF/EF (%) Winter 2007 147.5 20.2 0/15 0 (85-215) (17-23) Spring 2007 130.4 19.6 0/5 0 (122-144) (19-20) Summer 2007 - - - - Autumn 2008 179.8 21.2 13/15 86.6 (132-254) (18-23) Winter 2008 144.0 19.8 5/5 100 (108-178) (18-22) Seasons TNP Mean intensity Mean abundance Winter 2007 0 0 a 0 Spring 2007 0 0 a 0 Summer 2007 - - - Autumn 2008 157 12.0 [+ or -] 4.1 bc 10.4 [+ or -] 3.7 b (0-53) Winter 2008 91 18.2 [+ or -] 7.6 c 18.2 [+ or -] 7.6 c (3-46) * Different letters indicate significant difference between months (p < 0.05). Table 4. Parasitological indexes([+ or -] standard error) and biometry of Hoplias malabaricus parasitized by Austrodiplostomum compactum from Parana river, region of Presidente Epitacio, Sao Paulo State, Brazil. Mean values and variation, between parentheses, of fish weight and length, infected fish/examined fish (IF/IE), prevalence, total number of parasites (TNP), mean intensity and range, between parentheses, and mean abundance. Fish Fish Prevalence Seasons weight (g) length (cm) IF/EF (%) Winter 2007 643.5 40.1 7/15 46.6 (410-1025) (35-47) Spring 2007 407.3 35.0 2/3 66.6 (250-580) (29-41) Summer 2007 - - - - Autumn 2008 729.0 40.3 5/6 83.3 (394-1022) (32-46) Winter 2008 609.5 39.5 3/4 75.0 (360-782) (35-44) Seasons TNP Mean intensity Mean abundance Winter 2007 247 35.2 [+ or -] 6.9 16.4 [+ or -] 1.7 (0-57) Spring 2007 26 13 [+ or -] 11.1 8.6 [+ or -] 7.8 (0-24) Summer 2007 - - - Autumn 2008 68 13.6 [+ or -] 6.6 11.3 [+ or -] 5.9 (0-38) Winter 2008 214 71.3 [+ or -] 57.4 53.5 [+ or -] 43.5 (0-184) Table 5. Parasitological indexes ([+ or -] standard error) and biometry of Cichla sp. parasitized by Austrodiplostomum compactum from Parana river, region of Presidente Epitacio, Sao Paulo State, Brazil. Mean values and variation, between parenthesis, of fish weight and length, infected fish/examined fish (IF/IE), prevalence, total number of parasites (TNP), mean intensity and range, between parentheses, and mean abundance. Fish Fish Prevalence Seasons weight (g) length (cm) IF/EF (%) Winter 2007 450.6 29.7 3/13 23 (225-2365) (26-53) Spring 2007 311.3 29 2/3 66.6 (296-320) (28-30) Summer 2007 - - - - Autumn 2008 378.5 30.2 7/7 100 (140-498) (22-33) Winter 2008 - - - - Seasons TNP Mean intensity Mean abundance Winter 2007 4 1.3 [+ or -] 0.3 0.3 [+ or -] 0.2 a (0-2) Spring 2007 17 8.5 [+ or -] 6.5 5.6 [+ or -] 4.7 ab (0-15) Summer 2007 - - - Autumn 2008 50 7.1 [+ or -] 3.3 7.1 [+ or -] 3.3 b (1-21) Winter 2008 - - - * Different letters indicate significant difference between the months (p < 0.05). Table 6. Parasitological indexes and sites of infection of Austrodiplostomum compactum collected in fishes from Brazil. Hosts n p (%) MI Anostomidae Schizodon borellii 15 6.6 - Auchenipteridae Auchenipterus osteomystax 2 50.0 - Characidae Serrasalmus maculatus 3 33.3 - Cichlidae Cichla monoculus 40 65.0 7.8 C. monoculus 136 5.2 2.7 C. ocellaris 80 56.2 6.0 C. ocellaris 66 12.5 3.5 Cichla sp. 23 52.1 5.9 Cichlasoma paranaense 25 12.0 1.0 Crenicichla britskii 44 22.7 6.2 Geophagus brasiliensis 50 14.0 1.5 G. surinamensis 39 46.1 13.7 Satanoperca pappaterra 89 71.9 8.0 Curimatidae Cyphocharax Gilbert 60 1.7 1.0 Erythrinidae Hoplias malabaricus 198 11.1 1.4 H. malabaricus 27 66.6 32.6 Loricariidae Hypostomus regani 8 25.0 - Pimelodidae Conorhynchus conirostris 24 8.3 7.5 Pimelodus maculatus 82 17.0 1.0 Sciaenidae Plagiosaon squamosissimus 378 94.3 21.6 P. squamosissimus 61 92.6 39.0 P. squamosissimus 70 52.8 2.6 P. squamosissimus 81 95.0 38.9 P. squamosissimus 17 100.0 2-100 per eye P. squamosissimus 51 98.0 44.1 Hosts MA Site of infection Anostomidae Schizodon borellii 0.1 Aqueous humor Auchenipteridae Auchenipterus osteomystax 0.5 Aqueous humor Characidae Serrasalmus maculatus 0.3 Aqueous humor Cichlidae Cichla monoculus 5.1 Cranial cavity/vitreous humor C. monoculus 0.1 Eyes C. ocellaris 5.3 Eyes C. ocellaris - Eyes Cichla sp. 3.0 Crystalline Cichlasoma paranaense 0.1 Cranial cavity/vitreous humor Crenicichla britskii 1.4 Cranial cavity/vitreous humor Geophagus brasiliensis 0.2 Eyes G. surinamensis 6.3 Crystalline Satanoperca pappaterra 5.7 Cranial cavity/vitreous humor Curimatidae Cyphocharax Gilbert 0 Eyes Erythrinidae Hoplias malabaricus 0.1 Cranial cavity/vitreous humor H. malabaricus 20.5 Crystalline Loricariidae Hypostomus regani 0.1 Aqueous humor Pimelodidae Conorhynchus conirostris 0.6 Gills/Eyes Pimelodus maculatus 0.1 Eyes Sciaenidae Plagiosaon squamosissimus 20.2 Eyes P. squamosissimus 43.0 Eyes P. squamosissimus - Eyes P. squamosissimus 37.0 Cranial cavity/vitreous humor P. squamosissimus - Eyes P. squamosissimus 43.2 Crystalline Hosts Reference Anostomidae Schizodon borellii Yamada et al. (2008) Auchenipteridae Auchenipterus osteomystax Yamada et al. (2008) Characidae Serrasalmus maculatus Yamada et al. (2008) Cichlidae Cichla monoculus Machado et al. (2005) C. monoculus Machado et al. (2000) C. ocellaris Santos et al. (2002) C. ocellaris Martins et al. (2002) Cichla sp. Current study Cichlasoma paranaense Machado et al. (2005) Crenicichla britskii Machado et al. (2005) Geophagus brasiliensis Azevedo et al. (2006) G. surinamensis Current study Satanoperca pappaterra Machado et al. (2005) Curimatidae Cyphocharax Gilbert Abdallah et al. (2005) Erythrinidae Hoplias malabaricus Machado et al. (2005) H. malabaricus Current study Loricariidae Hypostomus regani Yamada et al. (2008) Pimelodidae Conorhynchus conirostris Brasil-Sato and Santos (2005) Pimelodus maculatus Bachmann et al. (2007) Sciaenidae Plagiosaon squamosissimus Paes et al. (2010) P. squamosissimus Santos et al. (2002) P. squamosissimus Martins et al. (2002) P. squamosissimus Machado et al. (2005) P. squamosissimus Kohn et al. (1995) P. squamosissimus Current study