Identification of Gyrodactylus (Monogenea, Gyrodactylidae) species in some of Southwest of Caspian Sea Basin fishes

Introduction

Members of the genus Gyrodactylus species are one of the extensive groups of monogenean ectoparasites with an elongated body which attaches to the host by means of a small organ called opisthaptor with sixteen marginal hooks and one pair of anchors connected by one dorsal bar and one ventral bar (Vanhove et., 2014). These parasites are hyperviviparous, which means that the embryos develop within each other inside the mother’s uterus and asexual reproduction alternates with sexual reproduction (Cable et al., 2002). It means that they experience only one adaptive barrier in their life. The direct life-cycle leads to auto-infection of the host. Despite detachment usually being fatal for the parasite (Bakke et al., 2007), gyrodactylid monogeneans which are detached from their host may form an important source of infection in fish communities. This is particularly significant for these ectoparasites, which have no specific free-living stage (Cable et al., 2002). Their hyperviviparous reproduction and monoxenous life cycle can lead to a sudden increase in worm numbers per host, particularly when the host densities are relatively high. Gyrodactylid monogeneans are frequently found on gills, skin and the fins of fishes (Shinn et al., 2010). They feed on the mucus and epithelial cells and can move freely on the host in almost a “caterpillar-like” fashion by alternatively attaching to the host’s epidermis with their posterior opisthaptor and anterior attachment glands. Many gyrodactylids exhibit distinct site preferences on the host but may display characteristic migrations on the host during their life cycle (Shinn et al., 2010). They parasitize marine, brackish and freshwater fishes and the lower aquatic invertebrates and usually have a narrow host range and are restricted to a single species, genus or family (Rhode, 1982; Noga, 2010).

In 50 years of research on the monogenean parasitic fauna of the fishes in Iran, only 14 species including Gyrodactylus cichlidarum Paperna, 1968 from Astronotus ocellatus; G. chinensis (Ling, 1962) from Carassius auratus; G. cyprini (Diarova, 1969) from Cyprinus carpio; G. derjavini (Mikhailov, 1975) from Salmo caspius and Oncorhynchus mykiss; G. elegans (Nordmann, 1832) from Abramis brama, Cyprinus carpio and Alburnus filippi; G. fossilis (Ergens, 1973) from Heteropneustes fossilis; G. gurleyi (Price, 1937) from Carassius auratus; G. kobayashii (Hukuda, 1940) from Carassius auratus and C. gibelio; G. mutabilitas (Bychowsky, 1957) from Capoeta gracilis; G. prostae (Ergens, 1963) from Rutilus kutum; G. shulmani (Ling, 1962) from Cyprinus carpio; G. sprostonae (Ling, 1992) from Arabibarbus grypus, Cyprinus carpio, Hypophthalmichthys molitrix and Hypophthalmichthys nobilis; G. stankovici (Ergens, 1970) from Cyprinus carpio and G. jalalii (Vanhove, Boger, Bukinga, Volckaerte Huyse et Pariselle 2012) from the only Iranian cichlid, Iranocichla hormuzensis have been described on the species level. Gyrodactylus jalalii (Mokhayer, 1981; Jalali et al., 1995; Papahn et al., 2004; Jalali and Barzegar, 2006; Jalali et al., 2007, Ebrahimzadeh Mousavi et al., 2009; Vanhove et al., 2012; Omidzahir et al., 2012; Ebrahimzade Mousavi et al., 2013; Omidzahir et al., 2015).  

Gyrodactylus species in low numbers may appear to have little effect on their hosts, but their mechanical and chemical stimulation do have an impact on the respiratory function of the gills and the skin, and also on the host’s ability to regulate its ion balance due to the puncture wounds inflicted by the attachment and the feeding of the parasites (Ferguson, 1989). Also, monogenean Gyrodactylids like the other parasites have proven useful in host identification, biogeography and evolutionary history, both at the interspecific (Pariselle et al., 2011; Gillardin et al. 2012; Muterezi Bukinga et al. 2012; Vanhove et al. 2013) and intraspecific (Vanhove 2014) level. The main objective of the present study is the identification and diagnosis of Gyrodactylus species from the native and exotic fishes in some rivers of the southern Caspian Sea basin in Mazandaran province.

Material and Methods

Study area and fish collection: Field investigations on the parasites of the fishes in some rivers of the southern Caspian Sea basin, in the Mazandaran province were carried out from March 2015 to June 2016. The fish samples were caught using a bag net, hook or electrofishing by local fishermen from different stations in Babolrud, Tajan, Shirud, Tonekabon, Nekarud, Siahrud, Haraz and Talar rivers. The fish samples were immediately transported alive in oxygen-filled plastic bags and then, sent to the parasitology laboratory, and wet mounts were prepared. Fish identification was performed by using keys of Berg (1965), Goad (2016) and Keivany et al (2017).

Parasitological study: Only fresh or already killed fish samples were subjected to the parasitological investigation. First, the fish samples were sedated by a drop of clove oil and then wet mount of fins, skin and gills were prepared and studied under a light microscope at 40X to 100x magnification. Vigorously moving Gyrodactylus worms were separated from the smears and subsequently fixed with ammonium picrate-glycerine (Malmberg, 1970) and mounted on a slide under a cover slip.

For the morphological study, the images of the opisthaptoral hard parts and the male copulatory organ (MCO) were captured at magnifications of 400X and 1000X oil immersion, using a digital microscope camera (Sony, SSC-DC80P), and the diagnostic variables were measured by Axiovision software (Carl Zeiss Vision AxioVision LE Rel. 4.5) on the captured images. The drawings of the taxonomic features were made from the captured images. A total of 18 morphological features were analyzed in this paper including body length (BL), body width (BW), diameter of haptor spherical (DHS), hamulus length (HL), hamulus shaft length (HSL), hamulus point length (HPL), hamulus process (HP), hamulus angle (HA), length of ventral bar (LVB), width of ventral bar (WVB), length of ventral bar membrane (LVBM), anterior bilateral processes of ventral bar (ABPVB), length of dorsal bar (LDB), width of dorsal bar (WDB), total length of marginal hook (TLMH), length of marginal hook sickle (LMHS), diameter of the male copulatory organ (DMCO) and greatest diameter of pharynx (GDP). All data are given in micrometers (μm) and are presented as a range and number of measurements (both in parentheses) preceded by the Mean ± Standard deviation. The identification and a comparison with the known species were based on Bychovskaya-Pavlovskaya et al., (1962); Yamaguti (1961); Gussev (1983) and Ergens (1983). Taxon and author names in this study were checked according to Coad (2016) and Eschmeyer (2017) for the hosts and Harris et al. (2008) and Shinn et al. (2010) for the gyrodactylids. 

Results

Approximately, 1240 fish specimens belonging to two families, nine genera and nine species were examined between March 2015 and June 2016. The list of fish species used for the parasitological study is given in Table 1.

Eleven Gyrodactylus species including Gyrodactylus mutabilitas, G. sprostonae, G. prostae, G. ctenopharyngodonis, G. gobioninum, G. katharineri, G. nemachili, G. proterorhini, G. ophiocephali, G. varicorhini and G. vimbi (Fig. 1) are isolated from skin (head, flank, operculum) and gills of the examined fishes from Babolrud, Tajan, Shirud, Tonekabon, Nekarud, Siahrud and Talar rivers belonging to the southern Caspian Sea basin. Parasites isolated from the studied fishes, the hosts and the infected organs are shown in Table 2. Gyrodactylus specimens have been described particularly in terms of size and morphological characters of the hamulus, the opisthaptor, the dorsal and ventral bars and other diagnostic variables.

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Table 3. Morphometric data of body: haptoral hard parts and male copulatory organ (MCO) of the described Gyrodactylus species, in μm (distances) or ° (angles), depicted as average ± standard deviation, with range and number of measurements in parentheses

Table 1. Examined native and exotic fish species in certain rivers in the southwest of Caspian Sea basin, Iran, studied during the period from 2015-2016

Table 2.  The Gyrodactylus parasite isolated from fishes in some rivers of the southernCaspian Sea basinin Mazandaran provincein the present study

Table 3. Morphometric data of body: haptoral hard parts and male copulatory organ (MCO) of the described Gyrodactylus species, in μm (distances) or ° (angles), depicted as average ± standard deviation, with range and number of measurements in parentheses

Table 3 (Continue d)

* body  length (BL), body width (BW), diameter of haptor spherical (DHS), hamulus length (HL), hamulus shaft length (HSL), hamulus point length (HPL), hamulus process (HP),  hamulus angle  (HA), length of ventral bar (LVB), width of ventral bar (WVB), length of ventral bar membrane (LVBM), anterior bilateral processes of ventral bar (ABPVB), length of dorsal bar (LDB), width of dorsal bar (WDB), total length of marginal hook (TLMH), length of the marginal hook sickle (LMHS), diameter of male copulatory organ (DMCO), greatest diameter