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

Document Type: Infectious agents- Diseases- Surgery

Authors

1 Department of Aquatic Animal Health and Disease, Faculty of Veterinary Medicine, University of Tehran .

2 Department of Aquatic Animal Health and Disease, Faculty of Veterinary Medicine, University of Tehran. Iran

3 3- Department of Aquatic Animal Health and Disease, Faculty of Veterinary Medicine, University of Tehran. Iran.

4 Department of Aquatic Animal Health and Disease, Faculty of Veterinary Medicine, University of Tehran

5 Faculty of Natural Resources sciences, Ghaemshahr Branch, Islamic Azad University

Abstract

BACKGROUND: Members of the genus Gyrodactylus species are one of the extensive groups of monogenean ectoparasites which parasitize marine, brackish and freshwater fishes. OBJECTIVES: The main objective of the present study is the identification and diagnosis of the Gyrodactylus specsies on the fishes in certain rivers in the southwest of the Caspian Sea basin. METHODS: The field investigations were carried out from March 2015 to June 2016 and approximately, 1240 fish specimens belonging to two families, nine genera and nine species from Babolrud, Tajan, Shirud, Tonekabon, Nekarud, Siahrud, Telar and Haraz rivers were examined. RESULTS: At least eleven Gyrodactylus species were isolated from skin and gills of the examined fishes. Among them, Gyrodactylus mutabilitas, G. sprostonae and G. prostae have been previously reported to be found in Iran. The rest, including Gyrodactylus ctenopharyngodonis, G. gobioninum, G. katharineri, G. nemachili, G. proterorhini, G. ophiocephali, G. varicorhini and G. vimbi are reported for the first time from Iranian Fishes. A tissue-specific microenvironment is seen in infection with Grodactylus proterorhini which was isolated from the gills, but mostly from the surface of the skin of Neogobius pallasi which is mainly specific to the brackish water of estuaries and coastal area. CONCLUSIONS: The host spectrum of Gyrodactylus species in Iran is actually wider and the further research may demonstrate that classification of individual species in terms of their host specificity will have to be changed and additional species of Gyrodactylus species would be found.

Keywords


Article Title [Persian]

فون انگل ژیروداکتیلوس (مونوژنه‌آ، ژیروداکتیلیده) ماهیان ایران در بخش جنوب شرقی حوضه آبریز دریای خزر

Authors [Persian]

  • مریم برزگر 1
  • حسینعلی ابراهیم زاده موسوی 2
  • هومن رحمتی هولاسو 3
  • علی طاهری میرقائد 4
  • عباس بزرگ نیا 5
1 گروه بهداشت و بیماری های آبزیان دانشکده دامپزشکی دانشگاه تهران، تهران-ایران
2 گروه بهداشت و بیماری های آبزیان دانشکده دامپزشکی دانشگاه تهران، تهران-ایران
3 گروه بهداشت و بیماری های آبزیان دانشکده دامپزشکی دانشگاه تهران، تهران-ایران
4 گروه بهداشت و بیماری های آبزیان دانشکده دامپزشکی دانشگاه تهران، تهران-ایران
5 گروه شیلات و آبزیان دانشکده منابع طبیعی، دانشگاه آزاد اسلامی واحد قائمشهر، قائمشهر، ایران
Abstract [Persian]

زمینه مطالعه: اعضاء جنس ژیروداکتیلوس ‌یکی از بزرگترین گروه‌های مونوژن انگل خارجی هستند که ماهیان دریایی، لب شور و شیرین را آلوده می‌نمایند. هدف: هدف اصلی مطالعه حاضر شناسایی و تشخیص گونه‌های ژیروداکتیلوس ‌ماهیان برخی رودخانه‌های بخش جنوب شرقی حوضه آبریز دریای خزر می-باشد. روش کار: تحقیقات در این زمینه از فصل بهار 1394 لغایت 1395 انجام شده و تقریباً 1240 نمونه ماهی متعلق به 2 خانواده، 9 جنس و گونه متفاوت از رودخانه‌های بابلرود، تجن، شیرود، تنکابن، نکارود، سیاهرود، تلار و هراز صید شده و مورد بررسی انگل شناسی قرار گرفتند. نتایج: در مجموع یازده گونه ژیروداکتیلوس از پوست و آبشش ماهیان مورد بررسی جدا شدند. در میان آنها، ژیروداکتیلوس موتابیلیتاس، ژ. اسپروستونه و ژ. پروسته قبلاً در ایران گزارش شده‌اند. باقی گونه‌ها شامل ژیروداکتیلوس کتنوفارینگودونیس، ژ. گوبیونینوم، ژ. کاتارینری، ژ. نماچیلی، ژ. پروتروهینی، ژ. اُفیسفالی، ژ. وریکورینی و ژ. ویمبی برای اولین بار از ماهیان ایران گزارش می‌شوند. همچنین ویژگی اندامی در آلودگی گاو ماهی شنی با گونه ژیروداکتیلوس پروتروهینی مشاهده گردید، اعضاء خانواده گاوماهیان خاص آب‌های لب شور مصبی و سواحل می‌باشد. نتیجه گیری نهایی: طیف میزبانی گونه‌های ژیروداکتیلوس در ایران وسیعتر از آنچه که اکنون به نظر می‌رسد بوده و ممکن است با انجام تحقیقات بیشتر در زمینه ژیروداکتیلوس‌های ایران، طبقه بندی گونه‌های مختلف از لحاظ ویژگی میزبانی تغییر کرده و گونه‌های جدیدی از این جنس پیدا شوند.

Keywords [Persian]

  • دریای خزر
  • ماهیان
  • ژیروداکتیلوس
  • رودخانهها

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.

.

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

Family

Scientific name

Weight (g)

Length (cm)

Number of examined specimens

Estimated   prevalence(%)

Cyprinidae 

Alburnoides bipunctatus (Bloch, 1782)

6.5 ± 1.4

8.7 ± 0.6

144

27%

Alburnus chalcoides (Güldenstaedt, 1772)

7.7 ± 0.9

7.56 ± .67

130

25%

Alburnus hohenackeri  (Kessler, 1877)

4 ± 1.3

7 ± 0.7

137

35%

Barbus lacerta (Heckel, 1843)

3.4 ± 0.4

7 ± 0.4

135

39%

Carassius gibelio (Bloch, 1782)

38 ± 7.1

14.6 ±    1.3

135

35%

Capoeta capoeta gracilis  (Keyserling, 1861)

33 ± 2.6

16.5 ± 2.4

138

24%

Squalius cephalus (Linnaeus, 1758)

6.2 ± 3.6

8.2 ± 1.9

148

44%

Vimba vimba  ­(Linnaeus, 1758)

24.4 ± 10

14 ± 1.2

140

24%

Gobiidae

Neogobius pallasi  (Berg, 1916)

6.3 ± 2.1

8.3 ± 1

133

19%

 

 

 

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

Parasite

Type host

Infection site

Type locality

Other host(s)

Gyrodactylus ctenopharyngodonis Ling, 1962

Barbus lacerta

Gills

Telar

Ctenopharyngodon   idella

Gyrodactylus gobioninum Gussev, 1955

                                            

Alburnus hohenackeri

 Capoeta Capoeta

 Squalius cephalus

Alburnoides bipunctatus 

Skin, Gills

Telar and Babolrud

Abbotina   rivularis, Gobio gobio, Gobio kessleri, Hemibarbus maculatus, Microphysogobio   amurensis, Pseudorasbora parva, Romanogobio tenuicorpus, Sarcocheilichthys   czerskii, Sarcocheilichthys sinensis

Gyrodactylus   katharineri ­Malmberg, 1964

vimba vimba

Capoeta capoeta

Gills and skin

Tonekabon and Telar

Alburnus alburnus, Aristichthys nobilis,   Barbus barbus, , Barbus meridionalis, Barbus peloponnesius, Capoeta capoeta,   Carassius auratus, Carassius carassius, Cyprinus carpio, Gobio gobio,   Hypophthalmichthys molitrix, Scardinius eryophthalmus

Gyrodactylus mutabilitas   Bychowskii, 1957

vimba vimba

Alburnus   hohenackeri

Skin

Telar and Shirud Rivers

Capoeta   capoeta

Gyrodactylus nemachili Bykhovskii, 1936

Capoeta   Capoeta

Gills and skin

Babolrud

Barbatula   barbatula, Triplophysa dorsalis, Triplophysa stoliczkae, Triplophysa strauchi

Gyrodactylus ophiocephali  Gussev, 1955

Squalius   cephalus

 

Gill, Skin

Tajan

Cyprinus carpio, Cyprinus carpio haematopterus

Gyrodactylus prostae Ergens, 1963

Alburnoides bipunctatus

Alburnus chalcoides

Carassius gibelio

Gills and skin

Tajan and Telar

Abramis ballerus, Abramis bjoerkna, Abramis brama, Leucaspius   delineatus, Leuciscus cephalus, Leuciscus idus, Leuciscus   leuciscus, Phoxinus phoxinus, Rutilus rutilus, Vimba vimba.

Gyrodactylus proterorhini Ergens, 1967

Neogobius pallasi

gills, skin

Tajan

Gobius cobitis, Gobius niger, Neogobius   melanostomus, Proterorhinus marmoratus, Zosterissesor ophiocephalus

Gyrodactylus   sprostonae Ling, 1962

Carassius gibelio

 Capoeta Capoeta

 Barbus lacerta

gills, skin

Babolrud, Telar and Tajan

Carassius carassius, Carassius gibelio,   Cyprinus carpio, Hypophthalmichthys molitrix Aristichthys hybrids,   Pseudaspius leptocephalus

Gyrodactylus varicorhini  Ergens et Ibragimov, 1976

Alburnoides bipunctatus

Skin

Telar

Capoeta   capoeta

 

Gyrodactylus  vimbi Schulman, 1953

vimba vimba

skin and gills

 

Tonekabon

Abramis   bjoerkna, Abramis brama, Abramis sapa, Alburnus alburnus, Barbus   meridionalis, Carassius carassius, Cyprinus carpio, Gobio gobio, Leuciscus   cephalus, Leuciscus leuciscus, Rutilus pigus. Rutilus rutilus. Scardinius   erythrophthalmus, Scardinius scardafa, Vimba vimba

 

 

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

Characteristic or features*

Gyrodactylus ctenopharyngodonis

Gyrodactylus gobioninum

 

Gyrodactylus katharineri

Gyrodactylus mutabilitas

 

Gyrodactylus nemachili

Gyrodactylus ophicephali

Gyrodactylus prostae

Gyrodactylus proterorhini

Gyrodactylus sprostonae

Gyrodactylus varicorhini

Gyrodactylus    vimbi

BL

229.5 ± 3.5

(227.1-232;   n=33)

251 ± 6.3

(245-260;   n=31)

1021.25 ±   28.7

(950-1075;   n=33)

347.6 ± 30.8

(320-390;   n=30)

186 ± 0.7

(186-187;   n=29)

656 ± 4.2

(653-659;   n=30)

350 ± 5.7

(340-350;   n=36)

533.13 ± 0.98

(532-533.7;   n=28)

270 ± 17.7

(250-300; n=40)

820 ± 22

(800-850; n=   33)

312 ± 10.4

(325-300; n=   5)

BW

41.6 ± 13.5

(32-51.2;   n=33)

82.5 ± 6.5

(75-90; n=31)

202.5 ± 8.5

(180-220; n=33)

128.22 ± 24.7

(100-160;   n=30)

92.8 ± 0.28

(92.6-93;   n=29)

201 ± 1.4

(200-202;   n=30)

98.33 ± 1.6

(95-100;   n=36)

132.5 ± 2.2

(130-133.8;   n=28)

81.16 ± 10.6

(67-92; n=40)

221 ± 15.5

(200-235;   n=33)

98 ± 9

(85-110;   n=31)

DHS

56 ± 0.3

(55.9-56.3;   n=33)

73.7 ± 4.7

(70-80; n=31)

167.5 ± 10.3

(150-190;   n=33)

70.39 ± 12

(55-80; n=30)

55.9 ± 0.07

(55.9-56;   n=29)

56 ± 1.4

(55-57; =30)

70 ± 2.9

(36-38; n=36)

63.3 ± 1.2

(62-64; n=28)

60 ± 3

(55-65; n=40)

171 ± 14.4

(150-180;   n=35)

67.6 ± 4.8

(60-73; n=31)

HL

54.2 ± 0.5

(53.8-54.5;   n=33)

58.75 ± 10.3

(50-70; n=31)

92.5 ± 7.7

(75-110;   n=33)

67.5 ± 6.4

(60-75; n=30)

53.5 ± 0.7

(53-54; n=29)

43 ± 0.0

(43; n=30)

37.16 ± 0.44

(36.5-38;   n=36)

48.9 ± 0.8

(48-49.4;   n=28)

48.7 ± 3.7

(45-55; n=40)

48.25 ± 2.4

(45-50; n=35)

59.8 ±  3.6

(58-62; n=31)

HSL

43.8 ± 0.8

(43.2-44.3;   n=33)

40 ± 4

(35-45; n=31)

67.5 ± 2.5

(46-42; n=33)

25 ± 0.8

(24-26; n=30)

44.7 ± 0.35

(44.5-45.1:   n=29)

32.5 ± 0.5

(32.1-32.8;   n=30)

31 ± 0.57

(30-32; n=36)

31.5 ± 1.3

(30-32.2;   n=28)

38.8 ± 1.8

(36-41; n=40)

38.75 ± 2.9

(35-42; n=35)

49 ±  3.6

(45-55; n=31)

HPL

23.9 ± 0.8

(23.3-24.5;   n=33)

20 ± 1.6

(18-22; n=31)

48.75 ± 1.4

(46-52; n=33)

23.75 ± 4.7

(20-30; n=30)

27.8 ± 0.35

(27.5-28;   n=29)

18.3 ± .4

(18-18.6;   n=30)

14 ± 0.57

(13-15; n=36)

23.6 ± 0.5

(23-23.9; =3)

19.5 ± 1.5

(18-22; n=40)

20 ± 1.6

(18-22; n=35)

29.8 ± 1.5

(28-32; n=31)

HP

̶̶

̶̶

̶̶

20.25 ± 1.7

(18-22; n=30)

̶̶

̶̶

̶̶

7.6 ± 0.6

(7-7.6; n=28)

̶̶

̶̶

̶̶

HA

63.7 ± 0.9

(63-64.3;   n=33)

38.25 ± 2.4

(35-40; n=31)

37.54 ± 0.65

(36-39; n=33)

41.7 ± 1.25

(40-43; n=30)

53.5 ± 0.7

(53-54; n=29)

28.5 ± 0.7

(19.5-29;   n=30)

59 ± 0.33

(59-60; n=36)

71.3 ± 1.2

(70-42; n=28)

70 ± 3.5

(65-75; n=40)

43.5 ± 2.4

(40-45; n=35)

40 ± 8.5

(39-40; n=31)

LVB

20.9 ± 0.4

(20.7-21.2;   n=33)

22 ± 2.5

(20-25; n=31)

49.5  ±   1.3

(47-53; n=33)

28.5 ± 2.6

(25-31; n=30)

23.5 ± 0.7

(23.2-24.1;   n=29)

19.8 ± 0.4

(19.5-20.1;   n=30)

9.66 ± 0.33

(9-10; n=36)

20.4 ± 0.4

(20-20.6;   n=28)

19.7 ± 1.4

(18-22; n=40)

19.75 ± 1.3

(18-21; n=35)

28.6 ± 2.3

(25-31; n=31)

WVB

4.4 ± 0.1

(4.3-4.5;   n=33)

5 ± 0.4

(4.5-5; n=31)

9.6 ± 0.24

(9-10; n=33)

8 ± 2.5

(5-10; n=30)

5.4 ± 0.1

(5.3-5.5;   n=29)

3.9 ± 0.14

(3.8-4; n=30)

4.66 ± 0.33

(4-5; n=36)

5.7 ± 0.6

(5-6; n=28)

2.9 ± 0.24

(2.5-3.2; n=40)

6.6 ± 1.1

(5.5-8; n=35)

6.7 ± 0.5

(6-7.2; n=31)

LVBM

15.1 ± 0.3

(14.9-15.3;   n=33)

17.24

29.5 ± 0.64

(28-31;n=33)

17.5 ± 2.4

(15-20; n=30)

13.6 ± 0.56

(13.2-14;   n=29)

19.3 ± 0.4

(19-19.5;   n=30)

0.01

11.13 ± 0.1

(11-11.2;   n=28)

̶̶

19.5 ± 1

(18-20; n=35)

22.16

Table 3 (Continue d)

Characteristic   or features*

Gyrodactylus   ctenopharyngodonis

Gyrodactylus gobioninum

 

Gyrodactylus   katharineri

Gyrodactylus mutabilitas

 

Gyrodactylus   nemachili

Gyrodactylus   ophicephali

Gyrodactylus   prostae

Gyrodactylus proterorhini

Gyrodactylus sprostonae

Gyrodactylus varicorhini

Gyrodactylus    vimbi

ABPVB

̶̶

3.75 ± 0.6

(3-4; n=31)

29.5 ± 0.3

(29-30; n=33)

1.9 ± 0.25

(1.5-2; n=30)

̶̶

13.2 ± 0.2

(13-13.3;   n=30)

̶̶

7.7 ± 0.2

(15-15.7;   n=28

̶̶

̶̶

5 ± 0.14

(4.8-5.2;   n=31)

LDB

15.8 ± 0.5

(15.4-16.1;   n=33)

19.7 ± 1.25

(18-21; n=31)

38.5 ± 1.2

(35-40; n=33)

21.75 ± 2.4

(20-25; n=30)

20.2 ± 0.4

(19.9-20.5;   n=29)

14.2 ± 0.2

(14-14.3;   n=30)

11 ± 0.57

(10-12; n=36)

15.5 ± 0.4

(15-15.7;   n=28)

9.7 ± 0.87

(8.5-11; n=40)

14.6 ± 1.1

(13-15.5;   n=35)

19.6 ± 1.5

(18-21; n=31)

WDB

1.8 ± 0.1

(1.7-1.9;   n=33)

2.1 ± 0.3

(1.8-2.5;   n=31)

1.9 ± 0.05

(1.8-2; n=33)

2.25 ± 0.6

(1.5-3; n=30)

1.95 ± 0.07

(1.9-2; n=29)

2.2 ± 0.1

(2.1-2.3;   n=30)

2.21 ± 0.16

(1.95-2.5;   n=36)

2.7 ± 0.2

(2.5-2.9;   n=28)

1.5 ± 0.16

(17-21; n=40)

3.8 ± 0.4

(3.5-4.3;   n=35)

2.5 ± 0.4

(2-3; n=31)

TLMH

24.9 ± 0.4

(24.6-25.2;   n=33)

20.25 ± 1.25

(19-22; n=31)

48.75 ± 1.3

(45-51; n=33)

33.7 ± 4.8

(30-40; n=30)

32.5 ± 0.7

(32-33.2;   n=29)

21.5 ± 0.7

(21-22; n=30)

48 ± 2

(44-50; n=36)

27.7 ± 0.6

(27-28; n=28)

19.2 ± 1.5

(17.21; n=40)

2.9 ± 0.33

(2.5-3.3;   n=35)

29.6 ± 1.2

(28-31; n=31)

LMHS

5.1 ± 0.2

(4.9-5.2;   n=33)

5 ± 0.4

(4.5-5.5;   n=31)

9.25 ± 0.5

(8-10; n=33)

10.25 ± 1.25

(9-12; n=30)

8.7 ± 0.4

(8.4-9; n=29)

4.7 ± 0.2

(4.5-4.8;   n=30)

8.46 ± 0.44

(7.5-9; n=36)

5 ± 0.7

(4.2 5.4;   n=28)

3.9 ± 0.3

(3.4-4.2; n=40)

29 ± 3.4

(25-33; n=35)

5.9 ± 0.3

(5.5-6.3;   n=31)

DMCO

10.4 ± 0.6

(10-10.8;   n=33)

10.37 ± 1.1

(9.5-12;   n=31)

29.25 ± 0.5

(28-30; n=33)

19.75 ± 1.25

(18-21; n=30)

̶̶

9.6 ± 0.1

(9.5-9.7;   n=30)

10 ± 0.00

(10; n=36)

̶̶

16.8 ± 1.7

(15-19; n=40)

11.25 ± 2.2

(9-14; n=35)

29.8 ± 1.5

(28-32; n=31)

GDP

20.5 ± 0.7

(20-21; n=33)

30.75 ±2.9

(28-35; n=31)

58.75 ± 0.75

(57-60; n=33)

20.25 ± 1.25

(19-22; n=30)

32.7 ± 0.35

(32.5-33;   n=29)

17.4 ± 0.5

(17-17.7;   n=30)

18.66 ± .088

(17-20; n=36)

51.3 ± 0.3

(51-51.5;   n=28)

23 ± 1.8

(20-25; n=40)

19.7 ± 1.25

(18-21; n=35)

19.6 ± 1.2

(18-21; n=31)

* 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


 

 

Discussion

 

Malmberg (1970) sub-divided the genus Gyrodactylus, based on the structure of the excretory systems, into six subgenera: G. (Gyrodactylus), G. (Mesonephrotus), G. (Paranephrotus), G. (Metanephrotus), G. (Neonephrotus) and G. (Limnonephrotus). Within each of these subgenera, Gyrodactylus species were classified based on their marginal hook morphology, host identity and site of infection. In 50 years of research on the monogenean parasitic fauna of the Iranian fishes, only 14 Gyrodactylus species were found, as the gyrodactylid parasites are notoriously difficult to identify owing to the heavy dependence on hook morphology, mainly morphometrics, but also made more difficult owing to a shape component (García-Vásquez et al., 2012). Further confounding factors are the considerable intra-species variation (Harris, 1998) and marginal hook variation that can arise due to abiotic factors such as water temperature and seasonality (Bakke et al., 2007). Furthermore, regarding the low outbreak of parasites in wild fishes (Kennedy, 2009), the extraction of sufficient DNA and subsequently molecular identification of the parasite would be difficult.

In the present investigation, 11 Gyrodactylus species were described, particularly in terms of size and the morphological characters of the hamulus, opistohaptor, the dorsal bar and other diagnostic variables from the different fishes in some rivers of the Caspian Sea basin. Among these 11 Gyrodactylus species, Gyrodactylus mutabilitas, G. sprostonae and G. prostae have been described previously in the context of Iranian freshwater fishes and the rest, including Gyrodactylus ctenopharyngodonis, G. gobioninum, G. katharineri, G. nemachili, G. proterorhini, G. ophiocephali, G. varicorhini and G. vimbi are reported for the first time in Iran. According to the Gyrodactylus database (Harris et al., 2008; Shinn et al., 2010), some fishes are introduced as new hosts for these species (Table 2). 

The Gyrodactylus species are remarkably host-specific and their specific host species and also the precise microhabitats on them are defined structurally, biochemically and physiologically such that they are almost identical in each specimen of a particular host species (Noga 2010; Sukhdeo and Bansemir, 1996). The ones with the widest host range included Gyrodactylus prostae and G. sprostonae. Gyrodactylus prostae has already been found on Carassius auratus and Rutilus frisii kutum (Jalali, 1998) and the present investigation added to the list three new host species including: Alburnoides bipunctatus, Alburnus chalcoides and Carassius gibelio. G. sprostonae was also found for the first time by Jalali (1998) in Cyprinus carpio, Hypophthalmichthys molitrix and Hypophthalmichthys nobilis in almost all fish farms in Iran and it seems this species is translocated by the introduction of the common carp and Chinese carp to Iran and now it is linked to the parasite fauna of the native fishes (Jalali, 1998).  In this paper, Capoeta gracilis and Carassius gibelio are introduced as new hosts for G. sprostonae in Iran. Gyrodactylus mutabilitas was formerly isolated from the gills of Capoeta capoeta (Jalali et al. 2007). In the present study, it was found on the gills and skin of two fish species from two different genus, Vimba vimba and Alburnus hohenackeri which shows its low host specificity.

Specific differences in the host fish epithelium and specific differences in the monogenean anterior adhesive, which contains mannose-rich glycoproteins, are implicated in stimulating the alternate complement pathway in the host and may all contribute to parasite-host specificity among the monogenean parasites (Buchmann, 1998b).

It is noteworthy that Gyrodactylus ctenopharyngodonis and Gyrodactylus varicorhini, both with two host species, have the narrowest host ranges.

The monogeneans live on the host’s epidermis; they live in its products (e.g. mucus), and feed on it. Some of the host products are “attractants” and may be inhospitable surfaces because of the immunological activity and therefore, tissue-specific microenvironment can be seen among Gyrodactylus species (Whittington et al., 2000). In the present study, Gyrodactylus proterorhini was isolated from the gills, but mostly from the surface of the skin of Neogobius pallasi with the prevalence and mean intensity of 34% and 1.2, respectively. Moreover, so far the parasites were only isolated from the members of Gobiidae family including Gobius cobitis, Gobius niger, Neogobius melanostomus, and Proterorhinus marmoratus. The gobies are a family found worldwide, mostly in warmer sea waters, although some species enter the brackish water of estuaries and coastal areas. The Neogobius pallasi were caught from the Mirud estuary (Talar river’s entrance to the Caspian Sea) with the salinity being around 12.5 ppt, which indicates that G. proterorhini is mainly specific to the brackish waters of coastal areas and estuaries. Here, Neogobius pallasi is considered as a new host for G. proterorhini.

The existing knowledge of the diversity, the host spectrum and the geographical distribution of the gyrodactylid monogenean parasites among the Iranian fishes is incomplete. Further studies should be carried out in order to identify and determine the species composition of the parasites in the different basins, their ecology and other biological specifications of the Gyrodactylus species in Iran. Also, an appropriate fixation and the processing of these monogenean parasites, as well as their molecular characterization, seem to be necessary requirements for providing new and reliable information. It is supposed that further research may demonstrate the host spectrum of Gyrodactylus species in Iran is actually wider and the classification of individual species in terms of their host specificity will have to be changed and additional species of Gyrodactylus species would be found.

 

Acknowledgments

 

The authors thank Miss Mitra Ghasemi for her assistance with the drawing of the taxonomic features of the parasites. We are very thankful to Dr. Furhan T. Mhaisen who extended great help in the research

 

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