SOME STUDIES ON MONOGENEA INFECTIONS IN GILLS OF MARINE WATER FISHES IN EGYPT

Document Type : Research article

Authors

1 1Department of Fish Diseases, Animal Health Research Institute, Mansoura Branch.

2 1Department of Fish Diseases, Animal Health Research Institute, Mansoura Branch. 1'2Department of Parasitology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516 Kafrelsheikh, Egypt.

Abstract

The present study was conducted to investigate the prevalence of monogenetic trematodes species. Clinical signs, lesions and pathological changes appeared on diseased fishes were caught from Ezbet Elborg area (in corresponding to Mediterranean Sea), Damietta province in Egypt. From 380 marine fish samples examined, 62 (16.31%) were positive for monogenetic trematodes. According to fish species, Abu Seif (Xiphian gladius) was the most infected 12/50 (24%), then Loot (Argyrosomus reguis) was 10/51 (19.6%), then Morgan (Pagellus erythrinus) was 25/144 (17.36%) and lastly Makarona (Saurida undoquamis) 15/135 (11.11%). Regarding monogenetic trematodes species were found to be most infected with more than one of monogenean species, Morgan (Pagellus erythrinus) 8/25 (32%) for (3) three infected monogeneans species while Loot (Argyrosomusregins) was infected with lowest monogenean species 2/10 (20%). Seven species of monogenetic trematodes infect the infested fish (Diplectanum aequans, Macrovavitrema Caballera and Choriocotyl hysterocha infected Morgan (Pagellus erythrinus)), (Microcotyle chrysophrii and Diplectanum jerbuae infected Makarona (Saurida undosquamis)), (Pseudaxine trachuri) infected Abu Seif (Xiphian gladius) and (Diplectanum serrani infected Loot (Argyrosomus regius). Seasonally, the highest infection of monogenean was in summer 23/85 (27.06%) and lowest infection in winter 10/100 (10%), also in spring 17/93 (18.28%) and autumn 12/102 (11.76%). The clinical signs detected on infected fish include loss of appetite, scratching, excessive mucous secretion, ulcers, hemorrhage and respiratory disorders. The pathological studies revealed severe pathological lesions, the changes include hyperplasia in mucous cells, necrosis of branchial epithelium and desquamation epithelial cells due to movement of parasites causing hemorrhage, edema and inflammatory reactions. This study highlights on the prevalence of monogenetic trematodes in some marine fishes in Egypt causing high economic loss in wild marine water fish.

Keywords


Assiut University web-site: www.aun.edu.eg

 

SOME STUDIES ON MONOGENEA INFECTIONS IN GILLS OF MARINE WATER FISHES IN EGYPT

 

RAWIA S.M. ADAWY1, REHAB R. ABD EL-MEGED1 and SOROUR, SH. S. GH1'2

1Department of Fish Diseases, Animal Health Research Institute, Mansoura Branch.

1Department of Parasitology, Animal Health Research Institute, Mansoura Branch.

1'2Department of Parasitology, Faculty of Veterinary Medicine, Kafrelsheikh University,

 33516 Kafrelsheikh, Egypt.

 

Received: 26 July 2016;  Accepted: 19 September 2016            

 

 

ABSTRACT

 

The present study was conducted to investigate the prevalence of monogenetic trematodes species. Clinical signs, lesions and pathological changes appeared on diseased fishes were caught from Ezbet Elborg area (in corresponding to Mediterranean Sea), Damietta province in Egypt. From 380 marine fish samples examined, 62 (16.31%) were positive for monogenetic trematodes. According to fish species, Abu Seif (Xiphian gladius) was the most infected 12/50 (24%), then Loot (Argyrosomus reguis) was 10/51 (19.6%), then Morgan (Pagellus erythrinus) was 25/144 (17.36%) and lastly Makarona (Saurida undoquamis) 15/135 (11.11%). Regarding monogenetic trematodes species were found to be most infected with more than one of monogenean species, Morgan (Pagellus erythrinus) 8/25 (32%) for (3) three infected monogeneans species while Loot (Argyrosomusregins) was infected with lowest monogenean species 2/10 (20%). Seven species of monogenetic trematodes infect the infested fish (Diplectanum aequans, Macrovavitrema Caballera and Choriocotyl hysterocha infected Morgan (Pagellus erythrinus)), (Microcotyle chrysophrii and Diplectanum jerbuae infected Makarona (Saurida undosquamis)), (Pseudaxine trachuri) infected Abu Seif (Xiphian gladius) and (Diplectanum serrani infected Loot (Argyrosomus regius). Seasonally, the highest infection of monogenean was in summer 23/85 (27.06%) and lowest infection in winter 10/100 (10%), also in spring 17/93 (18.28%) and autumn 12/102 (11.76%). The clinical signs detected on infected fish include loss of appetite, scratching, excessive mucous secretion, ulcers, hemorrhage and respiratory disorders. The pathological studies revealed severe pathological lesions, the changes include hyperplasia in mucous cells, necrosis of branchial epithelium and desquamation epithelial cells due to movement of parasites causing hemorrhage, edema and inflammatory reactions. This study highlights on the prevalence of monogenetic trematodes in some marine fishes in Egypt causing high economic loss in wild marine water fish.

 

Key words: Marine, Fish, Monogenea, gills, Egypt.

 

 


INTRODUCTION

 

Monogenean trematodes belong to one of the most species rich classes of fish parasites commonly found on fish gills and skin, and may lead to significant fish mortality as a consequence of tissue damage, respiratory distress and secondary bacterial and fungal infections. Many of their biological and ecological traits (Monoxeny, rapid reproduction, hermaphroditism) enable them to cause serious damage in both wild species and farmed stocks (Dezfuli et al., 2007; Lia et al., 2007; Stroma et al., 2010). Monogeneans  have high  host  specificity  and

 

 


Corresponding author: Dr. RAWIA S.M. ADAWY

E-mail address: Rawia_saad@hotmail.com

Present address: Department of Fish Diseases, Animal Health Research Institute, Mansoura Branch.

 

 

hence host specificity has often been used to estimate monogenean species richness as a function of fish biodiversity. Monogeneans are also very suitable for mathematical modeling in ecology (Whittington, 1998).

 

Monogenea is a class of Platyhelminthes parasites trematodes found mostly on external surfaces and gills of freshwater and marine fish (Whittington et al., 2004). Boeger and Kritsky (2001) recognized 53 families based on morphological characters. Most of monogeneans are highly host specific (Hargis, 1955 and Lawler 1981), which aids in the specific identification of worms from a particular host.

 

Parasitosis by monogenean trematode neobendenia melleni occurred in eight species of native marine fish held captive in the Bahamas. Clinical signs of the disease included reduced feeding, lethargy, cloudy eyes, discoloration, excessive mucous production, respiratory disorders and eventually death. This is the first report of N. melleni parasitosis in captive white grunts (Ilaemulon pluinieri), blue-stripped grunts (H. sciurus), and saucreye porgies (Calamus calamus). Tropical marine fish culture maybe constrained by N. melleni infections due to the pathogen's virulence and lack of host specificity (Karlw Mueller et al., 1994).

 

The monogenean parasites of red sea fishes of the gulf of Eilat and Suez at Israel and he collected and described ten Dactylogyridae from gills and skin of Littoral and reef fishes (Peperna, 1992). Among monogenea, nine species were observed, Tetrancistrum mugilis n. sp. Showed the highest average infestation rate (15-22%), Eichlidogyrus arthracanthus (9.68%), Lamellodiscus sp (7.72%), Diplectanum aequans (3.0%), D. Laubieri (2.3%), AL -lencotylaimami n. sp (1.01%), Microcotyle Chrysophrii (48%), Chorycotyle hysteroncha (0.33%), then Tareenia Suez Canali n. sp. (0.27%) (Ezz El-Dien, 1994).

 

Nouha Kaouachi et al. (2010) reported that a spatial distribution study of parasite populations of gills from 540 specimens belonging to Pagellus genus: Pagellus acarne, Pagellus erythrinus and Pagellus bogaraveo (Sparidae) was realized from the eastern Algeria coastline. A preliminary description allows the distinguishing of eight parasite species belonging to two subclasses: Monopisthocotylea and Polyopisthocotylea. Rates of parasite species and parasitic indices of host species were calculated. The study findings show that parasitic populations vary depending on the site and host species within the same genus.

 

Morsi et al. (2011) recorded that Benedenia; Capsalidae is a genus of important oral and cutaneous fluke parasite of aquarium, cultured and marine fish. Morphological and morphometric characterization of Benedenia sciaenae, a monogenean parasite infecting the gills of the brown-spotted grouper fish Epinephelus chlorostigma were described by means of light microscopy as a first description from Epinephelus chlorostigma. 215 out of 290 (74.1%) fish samples were found to be infected with this ectoparasitic capsalid causing pathogenic and epizootic events.

 

Nisreen Mahmoud et al. (2014) reported that this investigation was realized between December 2012 to November 2013. A total of 400 Sea bream (Sparusaurata) were sampled from a private fish farm in Ezbet Elborg area, Domietta province, Egypt and were investigated in terms of monogenean parasites. The prevalence, seasonal dynamics, mean intensity as well as the histopathological influence of the detected monogeneans were estimated. The standard parasitological methods were used in the survey and yielded four monogenean species on the Sea bream gills: Furnestinia Echeneis (58.59% of invaded fish), Encotyllable spari 32.81%, Sparicotlye chrysophrii 25.78% and Choriocotyle chrysophrii 17.19%. The total prevalence was 32% and the highest rate was recorded during summer. With the exception of Encotyllabe spari, the detected parasites are new records for the monogenean fauna in Egypt (new geographical record) and also Sea bream (Sparusaurata) is a new host record for the monogenean Choriocotyle chrysophrii.

 

The aim of this study is to investigate the effect of monogenetic trematodes on health of marine fishes.

 

MATERIALS AND METHODS

 

A total number of 379 fishes of Morgan (Pagellus erythrinus), Loot (Argyrosomus regius), Abu Seif (Xiphian gladius) and Makarona (Saurida undoquamis) were examined for monogeneans. Fishes were collected from two areas: Ezbet El Borg area (in corresponding to Mediterranean Sea,) Damietta province and Hurghada city, red sea in Egypt.

 

Samples were transported in water tanks supplied with oxygen to laboratory and kept alive in aquaria filled with the same water source and examined within few hours for investigation.

 

1-       Clinically: the clinical signs appeared on fish as movements of fish, operculum movements, skin, fins, eyes and gills colors.

 

2-       Parasitological examination:

Macroscopic examination: skin, surface, fins and gills were examined by naked eyes for detected lesions and changes due to parasitic infectionaccording to Markewitch (1976).

 

Microscopic examination: after removing opercula and exposing gill arches, each gill was removed carefully from fish, immersed in normal saline to remove any excess gill mucus.

 

Monogenean parasites were recovered with a Pasteur pipette using a dissecting binocular microscope. The monogeneans were fixed in 4% formalin and the worms were washed with distilled water to remove excess fixative. Worm identification were permanent whole mount preparation, some of the fixed and flattened specimens were stained with acid carmine followed by washing in ascending concentrations of ethyl alcohol series and then cleared in clove oil, xylene and then mounted with Canada balsm. (Ergens and Dulma, 1969). The cover slid prior to being examined under a light microscope.

 

3-       Histopathological examination:

The specimens from gills were fixed in 10% natural buffered formalin for routine histopathological examination. The fixed samples were washed in tap water overnight and exposed to ascending concentrations of ethanol (70, 80, 90 and 100%), cleared in xylene and embedded in paraffin. Tissue slides of sumtick sections were prepared and stained by hematoxylin and eosin (H&E).
The histopathological preparation was performed according to Bancroft (1996).

 

RESULTS

 

In this study clinical signs include lethargy, anoxia, loss of appetite and scratching Mucous secretion excess, opacity on gills and even ulcers, congestion and hemorrhages and may appear respiratory manifestations, gasping and death (Fig 1).

 

Out of total 380 examined samples of marine water fish include (Morgan (Pagellus erythrinus), Makarona (Saurida undoquamis), Loot (Argyrosomus regius) and Abu Seif (Xiphian gladius)), 62 (16.31%) were infested with monogenetic trematodes in gills. The prevalence of monogenean in different fish were the highest infestation present in Abu Seif (Xiphian gladius) fish (24%) while the lowest prevalence present in Makarona (Saurida undoquamis) (11.11%), also prevalence infestation in Loot (Argyrosomus regius) (19.6%) and (17.3%) in Morgan (Pagellus erythrinus) fish in table (2).

 

Types of monogenean parasites in different fish species were found to be Diplectanum aequans, Macrovalvitrema coballera and Choriocotyle hysteroncha in Morgan (Pagellus erythrinus). Microcotyle Chrysophrii and Diplectanum jerbuae infestation in Makarona (Saurida undoquamis). Psudaxin trachuri infestation in Abu Seif (Xiphian gladius). Diplectanum serrani infected Loot (Argyrosomus regius) in table (3).

 

Seasonally, the prevalence of monogenetic trematodes in examined fish were the high prevalence infection in summer season (27%) and spring season (18%) but lowest seasonal prevalence was in autumn (11%) and winter (10%). table (4).

 

The morphological description of detected monogenea species: seven species of monogenea detected in four fish species of marine water fishes.

 

Morphological description of the detected monogenean parasites in gills of examined fishes

Morphological description of the detected monogenean parasites in Morgan (Pagellus erythrinus):

 

1)       Diplectanum aequans. Wangener, 1857
Subfamily: Dactylogyidnea
Family: Diplectanidae
Site: gills
Fig: 2

 

Description:

A small monogenean with spined integument and measured 0.95-1.01 mm in length and 0.26-0.28 mm as maximum width. There were two pairs of eye spots, the posterior one was larger than the anterior lying in front of the large elongated pharynx which measured 0.06-0.07 by 0.06-0.08 mm. Also there were three pairs of adhesive head organs and two groups of gland cells which were ventrally located lateral to the pharynx (6-7 cells). The intestinal caeca run posteriorly without reaching the opisthaptor.

 

2)       Macrovalvitrema caballero et Bravo Hollis, 1955
Family: Macrovalvitrematidae:
Site: gills
Fig: 3

 

Description:

Body nearly cylindrical smooth, prhaptor large, shaped like a wide goblet with two large oral suckers bottom. Opisthohaptor attached obliquely to attenuated posterior end of body proper with 8 large clamps arranged in two longitudinal groups, one group of two suckers dorsal, on the peduncle formed by prolongation of haptor, the other group ventral, each clamp guitar – shaped, with two subequal valves constricted toward middle. Each valve bears at its base a completely sclerotized transverse sclerite which articulates with lateral marginal sclerites as well as median sclerite. At the constricted part there are two more sclerites, a transverse and longitudinal, former reaching to, but not articulating with, the median sclerite, latter long, extending from basal sclerite to near distal end of valve, parallel to short above mentioned marginal sclerite which terminates in a recurved hook. One of the valves terminates in muscular, lobed membrane. At the base of one dorsal clamp is a rudimentary larval haptor provided with two pairs of hooks. Pharynx present behind prohaptor. Intestinal limbs with short lateral branches, united at anterior part of opisthohaptor into a single ramus which terminates dorsally near the posterior end of the body proper clamps are attached. Testes numerous, large, occupying postovarian median area. Genital pore behind pharynx, provided with a disc armed with radial hooks. Ovary pretesticular, in form of a shepherd's crook. Vagina large, dorsal, midway between genital disc and ovary. Viellaria extending from in front of genital disc to beyond cecalunion. parasites of marine teleosts. Type species: M. Sinaloense Caballero et Brave Hallis, 1955 (p 1.50, Fig 335, on gills of Micropogonectenes, Mazatlan, Sinaloa, Oceanopacific et al. Norte. 1.82 mm.

 

3)       Choriocotyle hysteroncha, Fujii, 1944
Subfamily: charicotylinae
Family: Diclidophoridae
Site: gills
Fig: 4

 

Description:

It had elongated body with attenuated anterior end and it measured 2.9 – 3.4 mm length by 0.64 – 0.66 mm as maximum width. The prohaptor had one pair of suckers each was 0.54 – 0.62 mm by 0.038 – 0.096 mm. pharynx was large 0.062 – 0.077 mm by 0.077 – 0.092 mm. the genital pore was median in the region of oesophageal bifurcation and armed with six to eight hooks of 0.016 – 0.02 mm long. Testes were smooth, median post ovarian and 16-20 in number ovary was median, equatorial with pre ovarian seminal receptacle. Vitelline follicles filled most of the body from the level of genital pore till the opisthaptor. Vagina was absent. The opsthaptor measured 0.56 – 0.62 mm long with four pairs of pedunculated clamps, each of 0.16 – 0.18 mm long by 0.21 – 0.25 mm wide. There was a short terminal lappet lying between the last pair of haptoral pedicles bearing two pairs of anchors. The lamps had chitinious pieces and curved lateral bars, while their musculature was asymmetrical.

 

Morphological description of the detected monogenean parasites in Abu Seif (Xiphian gladius):

Pseudaxine trachuirparona (Perugia, 1889 and Price, 1943)

Subfamily: Dactylogyridae
Site: gills
Fig: 5

 

Description:

Body 5 – 6 mm long, 2 – 2.5 mm wide. Haptor unilateral, with a single row of clamps on its oblique lower edge, terminal lappet with one pair of anchors. Cephalic region on bearing a pair of buccal suckers. Testes numerous, post ovarian. Ovary V – shaped with unequal arms.

 

Morphological description of the detected monogenean parasites in Makarona (Saurida undoquamis):

Microcotyle Chrysophrii (Von Beneden and Hesse, 1863)

Subfamily: microcotylinae
Family: microcotylidae
Site: gills
Fig: 6

 

Description:

It has lancelated body of 4.70 – 4.90 mm length and 0.50 – 0.56 mm as maximum width at the middle of the worm. Anteriorly, there were a pair of buccal suckers each has a septum and numbers of minute spines. The muscular pharynx was spherical measuring 0.038 – 0.044 mm by 0.044 – 0.048 and away by 0.076 – 0.082 mm from the anterior margin of the worm, following by the oesophagus with two lateral diverticula. The intestinal ceaca bifurcated anterior to the genital atrium and extended posteriorly with inner and outer diverticula till reaching about the level of the haptor. Testes were ovoid, numerous, vary in numbers (12-18) lying in posterior mid region of the body each measured 0.076 – 0.093 by 0.07 – 0.08 mm. the muscular copulatory organ was ovoid in shape. Genital atrium measured 0.10 – 0.12 by 0.12 – 0.13 mm armed with 32 – 38 spines with pointed curved tips, four of them located centrally. The length of spines was 0.18 – 0.51 mm. ovary was pretesticular and v shaped and its extremities directed backward, the genito-intestinal canal cross the ovary. Vitellaria were follicular and coextensive with intestine. The opithaptor was triangle in profile and bordering with a row of numerous (65-70) pairs of small clamps of uniform structure. No terminal anchors or marginal hooklets were present.

 

Diplectanum jebuae (Bychowsky, 1933)
Subfamily: Ancyrocephallinae
Family: Dactylogridae
Site: gills
Fig: 7

 

Description:

Flukes of small size. Head region not clearly demarcated. Head organs 3-4 pairs. Eyes 2 pairs. Cephalic gland cells in two groups. Pharynx oval in shape, muscular. Oesophagus very short. Intestinal crura extending posteriorly up to a little behind the testis. Opisthaptor consists of two lateral transverse bars, one median transvers bar, two pairs of anchors and dorsal and ventral squamodiscs. Each squamodics with 18-20 rows of arc – shaped lamellae. Each lamella best with samm know like outgrowths, projecting downwards. Marginal hooklets 4-5 pairs present. Ovary median, rounded to oval and pretesticular. Vittelaria well developed, occupying most of the available space in the post bifurcal zone. Testis single, median, rounded to spherical and post ovarian. Vas deferens, short and narrow forming seminal vesicle. Cirrus tubular and bipartite with an accessory piece. Genital pore rounded and post bifurcal. Prostate glands seen at the base of seminal vesicle, scattered irregularly. Body length including opisthaptor 0.775 – 0.821 mm. width across the ovarian region 0.17-0.201 mm. pharynx 0.048-0.056 x 0.56-0.060 mm. opisthaptor 0.142 – 0.144 mm wide. Squamodise 0.06-0.065 x 0.088 – 0.090 mm wide. Median transverse bar 0.06 – 0.080 mm wide. Dorsal anchors length 0.032 – 0.036 mm. ventral anchor length 0.04 – 0.052 mm. marginal hooklet length 0.01 mm. ovary 0.032 – 0.040 x 0.060 – 0.080 mm. testis 0.080 x 0.048 – 0.068 mm. cirrus width 0.11 – 0.125 mm.

 

Morphological description of the detected monogenean parasites in Loot (Argyrosomus regius):

Diplectanum serrani (Yamaguti, 1952)

Site: gills

Fig: 8

 

Description:

Body elongated lanceolate, with haptor well-marked off, 0.45 – 0.66 mm in length, 0.1 – 0.14 mm in maximum width at or near level of genital pore or ovary and testis. Posterior part of body covered dorsal hook 33-54 μ long from end of ventral root to height of curve of blade, rosal root nodular; ventral hook 42 – 49 μ long from end of dorsal root to height of curve of blade, ventral root nearly as long as dorsal one, but more attenuated distally; connecting rod 48 – 54 μ long, swollen at inner end; central bar 75 – 90 μlong by 12 – 20 μ wide, blunt-pointed at both ends. Marginal hooklet 8 – 9 μ long. Squamodisc 39 – 45 μlong by 33 – 42 μ wide, consisting of 9 – 11 concentric rows of scales.

 

Head triangular or trapezoidal, 48 – 70 μ wide at base, with three pairs of swollen sticky gland ducts on each side. Two pairs of eye spots in front of pharynx. Sticky glands well developed on either side of eye spots and pharynx. Pharynx 27 – 33x21 – 27. Esophagus very short, ceca extending some distance further back of testis and terminating blindly.

 

Testis oval, 35 – 63x 24 – 42 μ, situated at about midbody. Vas deferens narrow, running forward along uterus on its sinistrodorsal side, forming a small fusiform vesicular seminalis; dutcus ejaculatorus very narrow, looped in front of vesicular seminalis; muscular bulbus ejaculatorius as observed in D. epinepheli Yamaguti, 1938 has not been detected. Copulatory organ 60 – 70 μ long, consisting of a reniform, chitinous structure, which is divided into four com-partments, and whose posterior end is produced into a styliform process, and a fine tubular cirrus proper, whose end is usually more or less winding. The thing-walled muscular sheath enclosing the cirrus proper runs arcuately toward the genital pore and opens along with the uterus. Genital pore ventral to posterior end of prostatic reservoir. Latter elongate sacuular, 30 – 40x 15 – 22 μ, along right side of reniform portion of copulatory organ, into which it opens at the anterior end. Prostate cells extending in dorsal are between copulatory organs and ovary, though not illustrated in the figure.

 

Ovary 30 – 58x24 – 50 μ, turning round right cecum, with the attenuated distal portion ventral to the anterior end of the main part, which lies immediately aterodextral to the testis. The uterus, receiving the shell gland and the seminal receptacle at the very beginning, is provided with fine circular muscle fibers and runs a little obliquely forward. No mature eggs observed. Vagina short cylindrical, opening in left submedian line a little behind genital pore, chitinized at its posterior somewhat swollen part, from which the winding half-chitinized vaginal duct is continued backward. The straight posterior portion of the vaginal duct is however no more chitinous and forms a small receptaculum semins at its posterior end. Vitelline follicles extending from pharynx to cecal ends.

 

 

 

 

Table 1: Size and length of different types of examined fishes.

 

Type of examined fish

Length (cm)

Weight (gm)

number

Morgan (Pagellus erythrinus)

10 – 12 cm

13 – 15 cm

144

Makarona (Saurida undoquamis)

11 – 13 cm

10 – 12 cm

135

Loot (Argyrosomus regius)

70 – 75 cm

1000 – 1500 cm

51

Abu Seif (Xiphian gladius)

100 – 120 cm

1000 – 1500 cm

50

 

Table 2:Prevalence of monogenean parasites in different species of marine fishes.

 

Fish species

No. of exam. Fish

No. of infe. Fish

% of inf. Fish

Pagellus eryrhinus

144

25

17.36

Makarona (Saurida undoquamis)

135

15

11.11

Loot (Argyrosomus regius)

51

10

19.60

Abu Seif (Xiphian gladius)

50

12

24

Total

380

62

16.31

 

Table 3:Types of monogenean parasites in different infested fish species.

 

Fish species

Parasites species

Morgan (Pagellus erythrinus)

  • Diplectanum aequans
  • Macrovalvitrema coballera
  • Choriocotyle hysteroncha

Makarona (Saurida undoquamis)

  • Microcotyle Chrysophrii
  • Diplectanum Jerbuae

Abu Seif (Xiphian gladius)

  • Psudoxine trachuri

Loot (Argyrosomus regius)

  • Diplectanum serrani

 

Table 4:Seasonal prevalence of monogenean parasites in examined fishes.

 

Season

No. of exam

No. of infested fish

% of inf. Fish

Winter

100

10

10

Spring

93

17

18.28

Summer

85

23

27.06

Autumn

102

12

11.76

Total

380

62

67.1

 

 

Fig. (1): Pagellus erythrinus infected with Diplectanum aequans in gills

 

Fig. (2): Diplectanum aequans

 

A) The prohaptor; two pairs of eye spots, large elongated pharynx. B) Diplectanum aequans, full view. C) The opisthaptor; 3-7 pairs of small marginal hooklets, two pairs of Hamuli.

 

 

 

 

Fig. (3): Macrovalvitrema coballera

A) The prohaptor; wide goblet with two large oral suckers. B) Macrovalvitrema coballera, full view. C) The opisthaptor; 8 large clamps, one group of two suckers dorsally.

 

 

 

Fig. (4): Choriocotyle hysteroncha

A) The prohaptor; one pair of suckers, large pharynx. B) Choriocotyle hysteroncha, full view. C) The opisthaptor; four pairs of clamps.

 

 

 

Fig. (5): Psendaxine trachuri

 

A) The prohaptor; a pair of buccal suckers. B) Psendaxine trachuri, full view. C) The opisthaptor; single row of clamps on its oblique lower edge, terminal lappet with one pair of anchors.

 

 

 

Fig. (6): Microcotyle chrysophrii

A)      The prohaptor; a pair of buccal suckers, minute spines, muscular pharynx. B) Microcotyle chrysophrii, full view. C) The opisthaptor; triangular in profile with a row of numerous small clamps.

 

 

 

Fig. (7): Diplectanum Jerbuae

A) The prohaptor; 3 pairs of head organs, 2 pairs of eyes, cephalic gland cells, oval pharynx. B) Psendaxine trachuri, full view. C) The opisthaptor; two lateral transverse bars, one median transverse bar, two pairs of anchors, dorsal and ventral squamodiscs.

 

 

 

Fig. (8): Diplectanum Serrani

 

A) The prohaptor; triangular head, three pairs of gland ducts, two pairs of eye spots, marginal hooklet, squamodisc. B) Psendaxine trachuri, full view. C) The opisthaptor; dorsal hook, ventral root of curved blade, nodular dorsal root.

 

   

 

   

 

 

Fig. (9): hyperplasia, fusion and necrosis of gill filaments of gill, pagellus erythrinus infected with Diplectanum aequans

Fig. (10): Dilated branchial vessels and hyperplasia of gill lamellae due to infection with monogenean parasites with large number

Fig. (11): The edematous fluid together with inflammatory cells and dilation of branchial blood vessels

Fig. (12): Large number of mononuclear cells infiltration due to infection with monogenetic trematodes

 

 


Histopathological results:

The histopathological examination revealed hyperplasia of epithelium of gill filaments, inflammatory reactions, hemorrhage, destruction of gill tissues due to attachment of monogenean parasites with gill filaments by anchors. The infested gills show diffuse degeneration and necrosis in the filament epithelial tissues and dilated blood vessels. The parasites were easily detected in affected gills caused circumscribed area at sites of parasitic attachment. (Fig. 9).

 

The lesions contain mucous cells, hyperplasia, complete necrosis of branchial epithelium, hemorrhage, edema and desquamated epithelial cells were also observed. (Fig. 10).

The parasitic feeding on lamellar tissue were caused inflammatory reactions and fusion of secondary lamellae and proliferation of gill filaments caused mortality in infested fish. (Fig. 11) The gills were infiltrated with large number of eosinophilic granular cells due to monogenean infestation. (Fig. 12)

 

DISCUSSION

 

In the present study contribute important information on the parasite fauna of some species of salt water fish from Ezbet Elborg areas, Domietta province (corresponding to Mediterranean Sea) and Hurghada city, Red Sea in Egypt. The monogenean parasites were isolated from the gills of Morgan (Pagellus erythrinus) and identified as Diplectanum aequans, Macrovalvitrema coballera and Choriocotyle hysteroncha. Monogenean parasites were isolated from gills of Makarona (Saurida undoquamis) and identified as Microcotyle Chrysophrii and Diplectanum jerbuae. Monogenean parasites were isolated from Abu Seif (Xiphiangladius) and identified as pseudaxine trachuri. Also monogenean parasites were isolated from Loot (Argyrosomus regius) and identified as Diplectanum serrani. The morphological characteristics studied by light microscope.

 

The prevalence of monogenean parasites in Morgan (Pagellus erythrinus) was 17.36 this result agreed with (Nouha Kaouachi et al., 2010). The average infestation monogenean parasites in Makarona (Saurida undoquamis) was 26% these results not agreed with (Aida A. El Massry and Olfat, Mahdy, 1997).

 

While the average infestation in Abu Seif (Xiphian gladius) was 25%, this result agreed with (Malticucci et al., 2005) were reported the number species identified in the Mediterranean appears to be lower than these reported in Atlantic, on the other hand, the parasite fauna of the Mediterranean population to be represented mainly by specialist species such as the monogeneans Tristoma species. The monogenean parasites prevalence of Loot (Argyrosomus regius) were low (20%) these result agreed with (Merellaet al., 2009) were reported that two different batches of meager Loot (Argyrosomus regius) were stocked in the same floating cage located in north eastern Sardinia (western Mediterranean Sea). In total is 65 specimens meagre of both stocks were sampled for parasitological analysis present only 1 species of parasite, the microcotylid monogenean Sciaenacotyle panceri, was found on the gills of caged meagre.

 

Seasonally the monogenean parasites prevalence high in summer (27.6%) and spring (18.28%) but low in autumn (11.76%) and winter (10%) these results agreed with (Nisreen Mahmoud et al., 2014) were reported that the highest rate of infestation was recorded during summer (49%) while the lowest was during winter (19%). Regarding the monogenean worms and their morphological status it was noticed that, Diplectanum aequans (Wagener 1857, Diesing 1858) were collected from Morgan (Pagellus erythrinus) these result which agreed with Nisreen Mahmoud (1994). Concerning with Macrovalvitrema coballera were infested Morgan (Pagellus erythrinus) was morphological similar to those described by Yamaguti (1963). The presence of Choriocotyle hysteroncha in Morgan (Pagellus erythrinus) collected from Mediterranean Sea water were recorded by Fuji (1944) and Kohn et al. (1984). This result disagreed Nisreen Mahmoud (1994) were reported Choriocotyle hysteroncha in Parusauratus collected from Suez Canal water. Morphologically it agreed with of materials of Kohn et al. (1984) and Nisreen Mahmoud et al. (2014). Microcotyle Chrysophrii (Beneden and Hesse, 1863) was collected from Makarona (Saurida undoquamis) from Mediterranean Sea and morphologically which agreed with Nisreen Mahmoud et al. (2014). Diplectanum jerbuae (Bychowsky 1933) was obtained from gills of Makarona (Saurida undoquamis). Such recorded among the marine fishes could attributed in the workers' opinion and according to Gupta et al. (1974) that this species was also found on the gills of Therapon jerbuae (Forskal). Diplectanum serrani in Loot (Argyrosomus regius) collected from Mediterranean Sea. Morphologically, it agreed with materials of Yamaguti (1952).

 

The histopathological study revealed that Morgan (Pagellus erythrinus) infested with Diplectanum aequans showed proliferative bronchitis characterized by large number of mononuclear cells infiltration together with fusion and adhesion between the gills lamellae, lamellar edema was noticed where the interlamellar spaces revealed accumulation of edematous fluid together with inflammatory cells and dilation of branchial blood vessels. The proliferation and adhesion between gill lamellae attribute to mechanical injury of infested parasite and the edematous fluid together with inflammatory cells and dilation blood vessels indicates the chemical toxins released from parasite. Therefore, the tissue reaction in our study may be resulted from the defense mechanism of the host against monogenean parasites. These results were agreed with the findings of Paperna (1991), Eid (1997), Abd El-Rhim (1998) and Floravanti et al. (2006).

 

The infestation with monogenean parasites showed characteristic eggs or larvae embedded in the bronchial tissue, this result was in parallel with the finding of Whittington (1990) and Nisreen Mahmoud et al. (2014). Also, the gills were infiltrated with large number of eosinophilic granular cells (EGC) and degranulation of some cells. However, the role of EGC in defense mechanism still obscure, these results agreed with Roberts (1978) and Rawia Adawy (2000).

 

ACKNOWLEDGMENT

Our sincere gratitude to Dr. Nesma Rasheed, a pathology researcher, for helping us conducting pathological studies, providing us with references and extending the scope of our research.

 

 

REFERENCES

 

Abd El-Rahim, G.E.A. (1998): studies on the main parasitic diseases affecting cultured dish and its influences by some ecological factors. Ph.D. Thesis, Fac. Vet. Med. Zagazig. Univ. Egypt.

Aida A. El Massry and Olfat A. Mahdy (1997): The fish Makaronhi Seuzi (Saurus Tumbil) as new host record for some monogenean parasites in Egypt. Egypt. J. Med. Sci. 18 (2) December, 1997: 493-505.

Alvarez-Pellkero P. (Ed.); Baija J.L. (Ed.); Pasurco B. (Ed.); Berthe F. (Ed.,); Toranzo A.E. (Ed.); Mediterranean Agriculture Diagnostic Laboratories. Zaragoz E SIHEAM, (2004): P. 103 — 130 (options Mediterraneennes: Serie P. Etudes E recherches; no. 49(.

Bancroft, D.; Stevens, A. and Tumer, R. (1996): Theory and practice of histological techniques (2nd Edn) Churchill Living Stone. Edinburgh, London, Melbourne.

Boeger, W. andKrittsky, DC. (2001): Phylogenetic relationships of monogenoidea. In: D.T.J Littewood and R.A. Bray (Eds.), Interrelationships of the Platyhelminthes. Taylor and Francis, London and New York, 2001; pp. 92-102.

Bychowsky, B.E. (1933): Bemerkungenuber die monogeneatischen trematoden der Gattung Dactylogyrus (Dies, 1858.) Der in den tcichen des Shulz parkes des peterhofer Biologischen Institues Wohnenden Karauschen (Russian text) Trudy Leninger Obsh Estestyois Otded 2001. 62(3), 269-296.

Dezfuli, B.S.; Giari, L.; Simoni, E.; Menegatti, R.; Shinn, A.P. and Menera, M. (2007): Gill histopathology of cultural European seabass, Dicentrarchus labrax (L.), infected with Oiplectunum aequans (Wagener 1857) Diesing 1958 (Diplectanidae: Monogenea). Parasitol. Res. 100: 707-713.

Diesing, K.M. (1858): Revision des Myzhelminthen Abteilung: Trematoden. Sber. Akad. Wiss. Wien, 32 (21): 307-390.

Eid, S.A. (1997): studies on parasites of Egyptian cultured fish. M.V. Sctheseis Fac. Vet. Med. Cairo Univ.

Ergens, R. and Dulmaa, A. (1969): Monogenoidea from Cyprinus Carpio haematopterus and carassiusa uratus gibelia (Cyprinidae) from Monoglia, Folia parasitological (Praha); 16: 201-206.

Ezz El-Dien (1994): 'Studies on the ectoparasites on some marine water fishes in Sue Canal area. PhD degree. Vet. Parasitology. 1994.

Floravanti, ML.; Caffara, M.; Florio, D.; Gustinelli, A. and Marcer, F. (2006): Parasitic diseases of marine fish: epidemiological and Sanitary considerations Parassitologia 48: 15-18.

Fujii, H. (1944): Three monogenetic trematodes from mavrine fishes. J. Parastiol., 30: 153-168.

Gupta, N.K.; Khanna and Madhu (1974): On some of the monogenetic trematodes of marine fishes from Port-Blair (Andaman and Nicobar Islans, India) Part I. Rev. Iber. Parasiteol. Vol. 34 (3-4), 1974.

Hargis, W. (1955): A new species of Benedenia from Girella nigricans of opaleye. Journal of parasitology, 41: 40-50.

Kareem Morsy; Sayed Abdel-Monem; Fathy Abel-Ghaffar; Abdel-Rahman Bashtar; Ali Al-Ghamdi and Rania Abdel-Gaber (2011): First record of Benedenia sciaene (Monogenea: Capslidae) infecting the brown-spotted grouper fish Epinephelus chlorostigma (Family: Serranidae) from the Red Sea in Egypt. Life Science Journal, 2011; 8 (4).

Karl, W.; Mueller, W.; Ade. 0. Wtanapa and William D. (1994): Head; Occurrence and control of Neubenedenia melleni. (monogenea: Capsalidae) in cultured tropical marine fi including three new host records. Pages 140 - 142. The progressive fish culturist. 56, isssue 2.

Kohn, A.; Abrahson, B. and Macedo, B. (1984): Studies on some monogenean parasites Haemulensciurns (Shaw, 1803) (Pomadosyidae). J. Helminthol, J. Helminthol., 58: 213-218.

Lawler, AR. (1981): Zoogeography and host specificity of superfamily Capsalodiea Price, 1936 (Monogenea: Monopisthocatylea). An evaluation of the host-parasite locality records of superfamily capsaloidea price, 1936, and their utility in dterminations of host specificity and zoogeography. Special papers in Marine science No. 6, 650 pp. Gloucester point, Virginia, USA: Virginia Institute of Marine science and school of Marine Science, College of William and Mary 1981.

Lia, R.P.; Zizzo, N.; Tinelli, A.; Lionetti, A.; Cantacessi, C. and Oranto, D. (2007): Mass mortality in wild greater amberjack (Serioladumerili) infected by Zeuxapta Seriolac (Monogenea: Heteraxinidae) in the Iranian sea. Bull. Assoc. Fish. P. 27(3): 108-111.

Nisreen Mahmoud; Mahmoud, AM. And Fahmy, MM. (2014): Parasitological and Comparative pathological studies on monogenean infestation of cultured sea bream (Sparusaurata, Spariidae) in Egypt. Oceanography 2014, 2:4.

Nouha Kaouachi, Chahinez Boualleg, Mouran Bensouilah and Bernard Marchand (2010): Monogenean parasites in Sparid fish (Pagellus genus) in eastern Algeria coastline. African Journal of Microbiology Research Vol. 4 (10), pp. 989-993, 18 May 2010.

Paolo Merella; Santino Cherchi; Giovanni Garippa; Maria Letizia Fioravanti; Andrea Gustinelli and Fulvia Saloti (2009): Outbreak of Sciaenacotyle Panceri (Monogenea) on cage-reared meager Argyrosomus regius (Osteichthyes) from the western Mediterranean Sea. Diseases of Aquatic Organisms Vo. 86: 169-173, 2009.

Paperna (1991): Diseases caused by parasites the aquaculture of warm water fish. Annual Review of fish Diseases: 155-194.

Paperna, I. (1972): Monogenea red sea fishes. III Dectylogyridae from littoral and reef fishes. J. Helminthol. XL (1): 47 - 62

Price, E.W. (1962): North American monogenetic trematodes. XI. The family Heteraxinidae, J. Parasitol, 48: 402-418.

Rawia S. Adawy (2000): studies on the parastitic diseases of some freshwater fishes in Dakahlia Governorate. Ph. D. Vet. Sci (2000) Cairo Universtiy. Fac. of vet. Med. Dep. of Internal medicine infectious diseases and fish.

Roberts, R.J. (1978): Textbook of fish pathology. 1st edition, the pathophysiology and systemic pathology of hosts. BailliereTindall, Gassel LTD. C., London.

Simonetta Mattiucci; Valeria Farina; Alexandria Garcia; Miguel N. Santos; Loredana Mariniello and Giuseppe Nascetti (2005): Metazoan parasitic infections of swordfish (Xiphias Gladius L., 1758) From the Mediterranean Sea and Atlantic Gibraltar waters: Implications for stock assessment. Col. Vol. Pap. IccAT, 58 (4): 1470 – 1482.

Strona, G. Stefoni, F. and Galli, P. (2010): Monogeneidean parasites of Italian marine fish: and updated checklist. Ital. J. Zaol. 77(4): 419-437.

Von Beneden, P.J. and Hesse, C.E. (1863): Recherches sur les Bdellodes ou Hirudinees et les trematodes marins. Mem. A cad. Belg. Cl. Sci., 168p.

Wagener, G.R. (1857): Heminthologische Bemcrkungen aus einem Sendschreibcs an. C. Th. Von siebold. Z. Wiss. 2001., 9: 73-90.

Whittington, ID. (1990): The egg bundles of the monogenean Diochus remorae and their attachment to the gills fo remora, Echeneis naucrates. Int J Parasitol 20: 45-49.

Whittington, ID. (1998): Diversity down under; monogeneans in the Antipodes (Australia) with a prediction of monogenean biodiversity worldwide. Int. J Parastiol. 28: 1481-1493.

Yamaguti (1952): Parasitic Worms mainly from Celebes. Part 2.Monogenetic trematodes of fishes. Acto Medica Okayama volume 8, Issue 3.Art, I.

Yamaguti, S. (1963): Systema Helminthum. Vol. IV, Monogenea and Aspidocotylea John Wiley and Sons, Interscience Publishers New York; PP669.

Markewith, A.P. (1976): Parasitic copepodes of the fishes of the USSR. Translated from Russian published for Smithsonian Institution and the National Science Foundation, Washington D.C, by Indian National Scientific Documentation Center, Hillside Road, New Delhi.

Whittington, ID.; Deveney, MR.; Morgan, JAT.; Chisholm, LA. And Adlard, RD. (2004): A preliminary phylogenetic analysis of the capsalidae (platyhelminthes: Monogenea: Monopisthocotyles) inferred from large subunit rDNA sequences. Parasitology, 128: 511-519.

 

 

 

 

بعض الدراسات على الإصابة بديدان المونوجينيا التي تصيب خياشيم أسماک المياه المالحة في مصر

 

راوية سعد محمد عدوي ­، ريحاب رشاد عبد المجيد ، شيماء صبحي غريب

 

E-mail: Rawia_saad@hotmail.com             Assiut University web-site: www.aun.edu.eg

 

 

لقد تم فحص عدد (380) سمکة من أسماک الماء المالح وتشمل أسماک المرجان، أبو سيف، اللوت، المکرونة) لدراسة مدى تأثير الإصابة بديدان التريماتودا أحادية العائل (المونوجينيا) ولقد تم جمع الأسماک من عزبة البرج بمحافظة دمياط من مياه البحر الأبيض المتوسط في مصر وقد أثبتت النتائج أن أهم الأعراض الإکلينيکية والصفات التشريحية التي تم ملاحظتها على الأسماک المصابة کانت تشمل احتقان في الخياشيم مع زيادة إفراز السائل المخاطي على الخياشيم المصابة بالديدان وحيدة العائل (المونوجينيا) مع ضعف في شهية الأسماک وظهور مشاکل تنفسية على الأسماک المصابة وکانت نسبة الإصابة بين 380 من الأسماک المجمعة التي تم فحصها (16.31 %) إيجابياً. لقد أوضحت الدراسة وجود سبعة (7) أنواع مختلفة من ديدان المونوجينيا في مصر وکانت تلک الأنواع ديبليکتانم إکوانس، ماکروأوفالتريما کوبلايرا، کوريوکوتيل هاليسترونکا في أسماک المرجان بنسبة (17.36 %) ووجد ماکروکوتيل کوريوفري، ديبلاکتانم جريبي بنسبة (11.11 %) في أسماک المکرونة وأيضا وجد سيداکسين تراکيوري بنسبة (24 %) في أسماک أبو سيف وتم عزل ديبلوکتانم سيراني في أسماک اللوت بنسبة (19.60 %) وکانت أعلى نسبة إصابة بديدان وحيدة العائل (المونوجينيا) في أسماک أبو سيف (24 %) أما أقل نسبة إصابة کانت (11.11 %) في أسماک المکرونة. ولوحظ أن نسبة الإصابة بديدان وحيدة العائل مرتفعة في موسم الصيف والربيع (27 %) و (18 %) على التوالي وکانت نسبة الإصابة منخفضة في موسمي الخريف والشتاء (11 %) و (10 %) على التوالي. تبين وجود تغيرات باثولوجية واضحة في أنسجة خياشيم الأسماک المصابة بالديدان وحيدة العائل (المونوجينيا) في أسماک المرجان. هذه الدراسة تسلط الضوء على نسبة الإصابة من أنواع الديدان وحيدة العائل (المونوجينيا) المختلفة في أسماک الماء المالح في البحر الأبيض المتوسط في مصر وتفيد هذه النتائج الجديدة والحديثة في مقاومة هذا المرض.

REFERENCES
 
Abd El-Rahim, G.E.A. (1998): studies on the main parasitic diseases affecting cultured dish and its influences by some ecological factors. Ph.D. Thesis, Fac. Vet. Med. Zagazig. Univ. Egypt.
Aida A. El Massry and Olfat A. Mahdy (1997): The fish Makaronhi Seuzi (Saurus Tumbil) as new host record for some monogenean parasites in Egypt. Egypt. J. Med. Sci. 18 (2) December, 1997: 493-505.
Alvarez-Pellkero P. (Ed.); Baija J.L. (Ed.); Pasurco B. (Ed.); Berthe F. (Ed.,); Toranzo A.E. (Ed.); Mediterranean Agriculture Diagnostic Laboratories. Zaragoz E SIHEAM, (2004): P. 103 — 130 (options Mediterraneennes: Serie P. Etudes E recherches; no. 49(.
Bancroft, D.; Stevens, A. and Tumer, R. (1996): Theory and practice of histological techniques (2nd Edn) Churchill Living Stone. Edinburgh, London, Melbourne.
Boeger, W. andKrittsky, DC. (2001): Phylogenetic relationships of monogenoidea. In: D.T.J Littewood and R.A. Bray (Eds.), Interrelationships of the Platyhelminthes. Taylor and Francis, London and New York, 2001; pp. 92-102.
Bychowsky, B.E. (1933): Bemerkungenuber die monogeneatischen trematoden der Gattung Dactylogyrus (Dies, 1858.) Der in den tcichen des Shulz parkes des peterhofer Biologischen Institues Wohnenden Karauschen (Russian text) Trudy Leninger Obsh Estestyois Otded 2001. 62(3), 269-296.
Dezfuli, B.S.; Giari, L.; Simoni, E.; Menegatti, R.; Shinn, A.P. and Menera, M. (2007): Gill histopathology of cultural European seabass, Dicentrarchus labrax (L.), infected with Oiplectunum aequans (Wagener 1857) Diesing 1958 (Diplectanidae: Monogenea). Parasitol. Res. 100: 707-713.
Diesing, K.M. (1858): Revision des Myzhelminthen Abteilung: Trematoden. Sber. Akad. Wiss. Wien, 32 (21): 307-390.
Eid, S.A. (1997): studies on parasites of Egyptian cultured fish. M.V. Sctheseis Fac. Vet. Med. Cairo Univ.
Ergens, R. and Dulmaa, A. (1969): Monogenoidea from Cyprinus Carpio haematopterus and carassiusa uratus gibelia (Cyprinidae) from Monoglia, Folia parasitological (Praha); 16: 201-206.
Ezz El-Dien (1994): 'Studies on the ectoparasites on some marine water fishes in Sue Canal area. PhD degree. Vet. Parasitology. 1994.
Floravanti, ML.; Caffara, M.; Florio, D.; Gustinelli, A. and Marcer, F. (2006): Parasitic diseases of marine fish: epidemiological and Sanitary considerations Parassitologia 48: 15-18.
Fujii, H. (1944): Three monogenetic trematodes from mavrine fishes. J. Parastiol., 30: 153-168.
Gupta, N.K.; Khanna and Madhu (1974): On some of the monogenetic trematodes of marine fishes from Port-Blair (Andaman and Nicobar Islans, India) Part I. Rev. Iber. Parasiteol. Vol. 34 (3-4), 1974.
Hargis, W. (1955): A new species of Benedenia from Girella nigricans of opaleye. Journal of parasitology, 41: 40-50.
Kareem Morsy; Sayed Abdel-Monem; Fathy Abel-Ghaffar; Abdel-Rahman Bashtar; Ali Al-Ghamdi and Rania Abdel-Gaber (2011): First record of Benedenia sciaene (Monogenea: Capslidae) infecting the brown-spotted grouper fish Epinephelus chlorostigma (Family: Serranidae) from the Red Sea in Egypt. Life Science Journal, 2011; 8 (4).
Karl, W.; Mueller, W.; Ade. 0. Wtanapa and William D. (1994): Head; Occurrence and control of Neubenedenia melleni. (monogenea: Capsalidae) in cultured tropical marine fi including three new host records. Pages 140 - 142. The progressive fish culturist. 56, isssue 2.
Kohn, A.; Abrahson, B. and Macedo, B. (1984): Studies on some monogenean parasites Haemulensciurns (Shaw, 1803) (Pomadosyidae). J. Helminthol, J. Helminthol., 58: 213-218.
Lawler, AR. (1981): Zoogeography and host specificity of superfamily Capsalodiea Price, 1936 (Monogenea: Monopisthocatylea). An evaluation of the host-parasite locality records of superfamily capsaloidea price, 1936, and their utility in dterminations of host specificity and zoogeography. Special papers in Marine science No. 6, 650 pp. Gloucester point, Virginia, USA: Virginia Institute of Marine science and school of Marine Science, College of William and Mary 1981.
Lia, R.P.; Zizzo, N.; Tinelli, A.; Lionetti, A.; Cantacessi, C. and Oranto, D. (2007): Mass mortality in wild greater amberjack (Serioladumerili) infected by Zeuxapta Seriolac (Monogenea: Heteraxinidae) in the Iranian sea. Bull. Assoc. Fish. P. 27(3): 108-111.
Nisreen Mahmoud; Mahmoud, AM. And Fahmy, MM. (2014): Parasitological and Comparative pathological studies on monogenean infestation of cultured sea bream (Sparusaurata, Spariidae) in Egypt. Oceanography 2014, 2:4.
Nouha Kaouachi, Chahinez Boualleg, Mouran Bensouilah and Bernard Marchand (2010): Monogenean parasites in Sparid fish (Pagellus genus) in eastern Algeria coastline. African Journal of Microbiology Research Vol. 4 (10), pp. 989-993, 18 May 2010.
Paolo Merella; Santino Cherchi; Giovanni Garippa; Maria Letizia Fioravanti; Andrea Gustinelli and Fulvia Saloti (2009): Outbreak of Sciaenacotyle Panceri (Monogenea) on cage-reared meager Argyrosomus regius (Osteichthyes) from the western Mediterranean Sea. Diseases of Aquatic Organisms Vo. 86: 169-173, 2009.
Paperna (1991): Diseases caused by parasites the aquaculture of warm water fish. Annual Review of fish Diseases: 155-194.
Paperna, I. (1972): Monogenea red sea fishes. III Dectylogyridae from littoral and reef fishes. J. Helminthol. XL (1): 47 - 62
Price, E.W. (1962): North American monogenetic trematodes. XI. The family Heteraxinidae, J. Parasitol, 48: 402-418.
Rawia S. Adawy (2000): studies on the parastitic diseases of some freshwater fishes in Dakahlia Governorate. Ph. D. Vet. Sci (2000) Cairo Universtiy. Fac. of vet. Med. Dep. of Internal medicine infectious diseases and fish.
Roberts, R.J. (1978): Textbook of fish pathology. 1st edition, the pathophysiology and systemic pathology of hosts. BailliereTindall, Gassel LTD. C., London.
Simonetta Mattiucci; Valeria Farina; Alexandria Garcia; Miguel N. Santos; Loredana Mariniello and Giuseppe Nascetti (2005): Metazoan parasitic infections of swordfish (Xiphias Gladius L., 1758) From the Mediterranean Sea and Atlantic Gibraltar waters: Implications for stock assessment. Col. Vol. Pap. IccAT, 58 (4): 1470 – 1482.
Strona, G. Stefoni, F. and Galli, P. (2010): Monogeneidean parasites of Italian marine fish: and updated checklist. Ital. J. Zaol. 77(4): 419-437.
Von Beneden, P.J. and Hesse, C.E. (1863): Recherches sur les Bdellodes ou Hirudinees et les trematodes marins. Mem. A cad. Belg. Cl. Sci., 168p.
Wagener, G.R. (1857): Heminthologische Bemcrkungen aus einem Sendschreibcs an. C. Th. Von siebold. Z. Wiss. 2001., 9: 73-90.
Whittington, ID. (1990): The egg bundles of the monogenean Diochus remorae and their attachment to the gills fo remora, Echeneis naucrates. Int J Parasitol 20: 45-49.
Whittington, ID. (1998): Diversity down under; monogeneans in the Antipodes (Australia) with a prediction of monogenean biodiversity worldwide. Int. J Parastiol. 28: 1481-1493.
Yamaguti (1952): Parasitic Worms mainly from Celebes. Part 2.Monogenetic trematodes of fishes. Acto Medica Okayama volume 8, Issue 3.Art, I.
Yamaguti, S. (1963): Systema Helminthum. Vol. IV, Monogenea and Aspidocotylea John Wiley and Sons, Interscience Publishers New York; PP669.
Markewith, A.P. (1976): Parasitic copepodes of the fishes of the USSR. Translated from Russian published for Smithsonian Institution and the National Science Foundation, Washington D.C, by Indian National Scientific Documentation Center, Hillside Road, New Delhi.
Whittington, ID.; Deveney, MR.; Morgan, JAT.; Chisholm, LA. And Adlard, RD. (2004): A preliminary phylogenetic analysis of the capsalidae (platyhelminthes: Monogenea: Monopisthocotyles) inferred from large subunit rDNA sequences. Parasitology, 128: 511-519.