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Iheringia. Série Zoologia

Print version ISSN 0073-4721On-line version ISSN 1678-4766

Iheringia, Sér. Zool. vol.107  Porto Alegre  2017  Epub Oct 09, 2017

http://dx.doi.org/10.1590/1678-4766e2017026 

Articles

Myxobolus saladensis sp. nov., a new species of gill parasite of Mugil liza (Osteichthyes, Mugilidae) from Samborombón Bay, Buenos Aires, Argentina

Paula Marcotegui1 

Sergio Martorelli1 

1Centro de Estudios Parasitológicos y Vectores (CCT-La Plata), Boulevard 120 s/n entre av. 60 y calle 64 (1900) La Plata, Buenos Aires, Argentina.

ABSTRACT

Myxosporean Myxobolus saladensis sp. nov. in the gills of Mugil liza Valenciennes, 1836 from Samborombón Bay was described by light and electron microscopy studies. Spores were pyriform and binucleated, measuring 10.63±0.36 µm (n=20) long, 9.24±0.50 µm (n=20) wide and 4.13±0.36 µm (n=20) thick, included in polysporic cyst-like plasmodia. Elongated pyriform polar capsules were of equal size (3.84±0.27 µm long and 2.30±0.12 µm wide). The sporoplasm contained some sporoplasmosomes. Each PC contained a polar filament with 4-5 coils obliquely arranged in relation to the polar capsules axis. The PC wall was composed of two layers of different electron densities. Based on the morphological and ultrastructure differences of the spore to those of previously described species of Myxobolus, we describe a new species, Myxobolus saladensis sp. nov.

KEYWORDS Myxosporean; mullets; Myxobolidae; gills parasites

Members of Myxobolus Biitschli, 1882 are considered cosmopolitan, with many species cited in mullets. According to Zatti et al. (2015) approximately 90 myxosporean species have been identified in South America, of which 41 are from the this genus, mostly from Brazil (Eiras et al., 2010; Azevedo et al., 2010; 2011; 2012). Mullets live in shallow and brackish waters and are euryhaline, ranging from hypersaline lagoons to freshwater. They utilize estuarine nursery habitats where they feed largely on plant material obtained by grubbing through bottom detritus (Cervigón et al., 1993).

The Mugilidae is represented by three species along the coast of the Southwest Atlantic Ocean (Cousseau et al., 2005). In Argentine waters, the only mullet permanently present is the grey mullet Mugil liza Valenciennes, 1836 (see Cousseau et al., 2005) after synonymization of Mugil platanus Günther, 1880 with M. liza (Heras et al., 2009). This species is commercially exploited in Brazil and Argentina by inshore artisanal fisheries.

Helminths parasitizing M. liza have been reported by many authors in the last years (Knoff & Amato, 1992; Kohn et al., 1994; Knoff et al., 1997; Suriano et al., 2000; Carnevia & Speranza, 2003; Abdallah et al., 2009; Marcotegui & Martorelli, 2009a,b; Siquier & Ostrowski de Nuñez, 2009; Alarcos & Etchegoin, 2010; Martorelli et al., 2012). However, gill Myxozoa have not been reported from this host. Eiras et al. (2007) recorded Myxobolus platanus Eiras et al., 2007 parasitizing pancreatic tissue of Mugil platanus in Lagoa dos Patos, Brazil.

In a survey of fish parasites in estuarine areas of Argentina a new myxosporidian species was found in Mugil liza collected from Samborombón Bay. A light and electron microscopic study on the new species is presented.

MATERIALS AND METHODS

A total of 206 specimens of Mugil liza (Valenciennes, 1836) (Mugilidae) were captured between April 2006 and April 2009. These specimens ranging in total length from 2.8 to 32.0 cm and total weight from 0.22-331.41 g were captured from the mouth of the Canal Aliviador of Salado River (35°50’12.53”S, 57°25’22.28”W, Samborombón Bay, Buenos Aires, Argentina) and examined for parasites. Live fish were transported to the laboratory in containers filled with estuarine water and were kept alive in oxygenated aquaria until examination. Skin, fins, excised gills, and intestinal tract from newly killed fishes were analyzed under a dissecting microscope to detect parasites.

Plasmodium (Pmd) containing numerous spores were found in the gill filaments and gill rakers (Fig. 1). The gills infected were observed by DIC microscopy for fresh spore measurements. For ultrastructural studies, fragments of gills infected were excised and fixed in 2.5% Glutaraldehyde in 0.2 M Sodium Cacodylate buffer (pH 7.2) for 12 h at 4°C, washed in the same buffer 12 h at 4°C and post fixed in 2% OsO4 buffered with the same solution for 4 h at the same temperature. Ultrathin sections were observed in a JEOL 1200EX II TEM (JEOL Optical, Tokyo, Japan).

The dimensions of the spores (in µm) were expressed as the mean ±standard deviation. Length and width of spores were obtained from 20 fresh specimens. Thickness were obtained from 20 additional spores. Measurements of polar capsules length and width of the spores were obtained from ultrathin serial sections. All measurements were taken from microphotographs using Image J software (National Institutes of Health).

RESULTS

Myxobolus saladensis sp. nov.

(Figs 1-7)

Figs 1-4 Light and transmission electron micrographs of the myxosporean Myxobolus saladensis sp. nov. infecting gills and gills rakers of Mugil liza Valenciennes, 1836: 1, semithin section of a plasmodium; 2, isolated spores observed in differential interference-contrast (DIC); 3, ultrathin section of a plasmodium showing several spores at different levels (S); 4, sectioned spore showing the shell valves (V); polar capsules (PC); Sporoplasm (SP) and transverse section of the polar filament (arrows). 

Figs 5, 6 Myxobolus saladensis sp. nov. parasite of Mugil liza Valenciennes, 1836: 5, sectioned spore showing valves (V) and their suture lines (arrows), polar capsules (PC), different sections of the polar filaments (arrowheads) and some sporoplasmosomes (Sps); 6, detail of apical region of the PCs showing the PC wall (arrows) composed of two layers and the apical stopper (double arrows) and the different sections of the polar filament (arrowheads). 

Fig. 7 Schematic drawing of the morphology of a spore of Myxobolus saladensis sp. nov. witch infects Mugil liza Valenciennes, 1836 from Argentina.  

Diagnosis. Spherical Pmd containing numerous spores located in the gill filaments and rakers. Pyriform fresh spores tapering anteriorly 10.63±0.36 (range 10.05-11.13) µm long, 9.24±0.50 (range 8.42-9.79) µm wide, and 4.13±0.36 (range 2,65-4,9) µm thick. Two equal-sized pyriform PC measuring 3.84±0.27 (range 3.33-4.03) µm long and 2.30±0.12 (2.14-2.43) µm wide. Polar filament coiled in four or five turns.

Site of infection: spores located in epithelium of gill rakers.

Etymology. The specific epithet refers to the type locality, Salado River.

Type material. One glass slide with semithin sections of the cyst containing spores (Hapantotype) was deposited in the Museo de La Plata collection, number MLP-Pr-095.

Type Locality. Salado River, Samborombón Bay, Buenos Aires, Argentina.

Type Host: Mugil liza.

Prevalence: 12.7%.

Description. Spores typical of Myxobolus Bütschli, 1882, rounded in valvular view and biconvex in sutural view, shell valves smooth and without projections. Fresh mature spores pyriform in shape (Fig. 2). Mean spore measurements ± standard deviations as follows: 10.63±0.36 (range 10.05-11.13) long, 9.24±0.50 (range 8.42-9.79) wide, and 4.13±0.36 (range 2.65-4.91) thick. Spore wall thin and smooth comprising two symmetrical and equal shell valves adhering together along the prominent longitudinal sutural line (Figs 3-6). Internally, two equal and elongated pyriform polar capsules (PCs), located side by side at the same level, measured 3.84±0.27 (range 3.33-4.03) long, 2.30±0.12 (range 2.14-2.43) wide (Figs 3-6). Intercapsular appendix not observed. Inside the PCs, polar filament coil displayed four or five slightly oblique to the longitudinal axis (Fig. 6). Apical end of the PCs contained a circular stopper formed by electron-lucent material (Fig. 6). At the posterior pole of the spore, a binucleated sporoplasm contained numerous light vesicles, numerous sporoplasmosomes (Figs 4, 5).

Nuclei located at the same level, contained uniform chromatin without evident nucleoli (Fig. 3). A schematic drawing of spore morphology (Fig. 7) shows the arrangements of the different structures and organelles.

DISCUSSION

Of the Myxobolus species described from mullet, those analyzed during the present study resemble M. chiungchowensisChen, 1998, M. goensisEiras & D’Souza, 2004, M. goreensisFall et al., 1977, M. mugiliiHaldar et al., 1996, M. rohdeiLom & Dykova, 1994, and M. spinacurvaturaMaeno et al., 1990 from the size of spores. Nevertheless the new species proposed can be distinguished from M. chiungchowensis, M. goensis, M. goreensis, and M. mugilii, by having smaller size of the polar capsules, and M. spinacurvatura and M. rohdei by the number of turns of the filament polar capsules (see Tab. I).

Tab. I Comparative measurement (in µm) of the spores from Myxobolus spp. parasiting mugilid fishes which resembles the new species (SL, spore length; SW, spore width; PCL, polar capsules length; PCW, polar capsules width; NC, number of coils on the polar filament).  

Species SL SW PCL PCW NC Organ Host species
M. chiungchowensis 10.2-11.8 9.6-11 5.6-6.2 3.4-3.8 6-8 Intestine Mugil cephalus
M. goensis 9.5-10.5 6-7.5 4.5-6 2-3 5 Gills archs Mugil cephalus
M. goreensis 10-13 10-13 4-5 2-4 - Gills Mugil cephalus
M. mugilii 8.1-16.3 4-7.3 2.4-8.1 1.6-4 - Gills Mugil cephalus
M. rohdei 9.8-11.8 8.4-9.1 3.7-5 2.5-3.1 3-4 Kidneys Mugil cephalus
M. spinacurvatura 10.5-12.5 9-11 3.5-5 2.5-3.5 - Mesentery, brain, spleen Mugil cephalus
M. platanus 10-11 10-11 7-8 3.5-4 - Spleen Mugil platanus
M. galaxii 13-15 8.8-10 - - - All organs except gills Galaxias maculatus
M. magellanicus 11.9 ± 0.6 12.9 ± 0.5 3 - - Gills Galaxias maculatus
M. paranensis 12-15 7-8 6-7 2.5 - Gonads Salminus maxillosus
M. saladensis n. sp. 10.05±11.13 8.42-9.79 3.33-4.03 2.14-2.43 4-5 Gills Mugil liza

Eiras et al. (2007) reported Myxobolus platanus parasitizing pancreatic tissue of Mugil platanus (actually M. liza) in Lagoa dos Patos, Brazil. The new species differs from M. platanus by having smaller polar capsules not exceeding half the length of the spore (see Tab. I). Furthermore, the infection site (pancreatic tissue) of the parasite described by Eiras et al. (2007) differs from that of M. saladensis sp. nov., which infects gill rakers in M. liza.

In Argentina M. galaxii Szidat, 1953 and M. magellanicus Szidat, 1953 (Flores & Viozzi, 2001) have been reported from Galaxias maculatus Jenyns, 1842, and M. paranensis from Salminus maxillosus Bonetto & Pignalberi, 1965. The specimens studied can be distinguished from those species by having smaller spores (Tab. I). Additionally, Viozzi (1996) has reported Myxobolus sp. from Percichthys trucha Valenciennes, 1833, Galaxias maculatus and Hatcheria macraei Girard, 1855 in Patagonian lakes, and Sardella et al. (1998) reported Myxobolus sp. from Genypterus brasiliensis Regan, 1903 in Argentine Sea. In both reports, a formal description has not been undertaken, preventing a thorough comparison with the specimens found during this study.

According to Molnar (2002) knowledge of the actual site of establishment of the parasite in the gill may also facilitate the identification of parasite species; therefore, indicating the precise location of plasmodium development is indispensable for species descriptions. Host and organ specificity and tissue tropism should be considered in species identification (Liu et al., 2013). The new species plasmodium was found, in the epithelium of the gills rakers of all infected fish. The site of the plasmodium coincides with infections of the gill arch epithelium according to the typical localization of the plasmodium given by Molnar (2002).

Some gills Myxobolus species have been reported as pathogenic to fish (Camus & Griffin, 2010; Milanin et al., 2010; Liu et al., 2013). Heavy infections of myxozoan in gill lamellae, gills filaments or blood vessels of the gill arch, could produce severe gill changes affecting gas exchange. Although the new species is located in the epithelium of rakers this could affect the respiratory flow.

This is the second report of the genus Myxobolus from Mugil liza, and the fifth record of this genus in Argentina.

Acknowledgments

This work was funded by a fellowship grant from Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET) to P. S. Marcotegui, and a research grant from Universidad Nacional de La Plata (UNLP: N504) to S. R. Martorelli.

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Received: May 25, 2016; Accepted: August 10, 2016

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