1. bookVolume 58 (2021): Issue 2 (June 2021)
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Surface ultrastructure of the adult and juvenile stages of the trematode Astiotrema impletum (Looss, 1899) Looss 1900 (incertae sedis) from the Nile puffer, Tetraodon lineatus Linnaeus, 1758

Published Online: 08 Jun 2021
Page range: 188 - 195
Received: 23 Jul 2020
Accepted: 18 Feb 2021
Journal Details
License
Format
Journal
First Published
22 Apr 2006
Publication timeframe
4 times per year
Languages
English
Summary

A scanning electron microscope study was performed on the surface of the trematode Astiotrema impletum (Looss, 1899) Looss 1900 from the Nile puffer, Tetraodon lineatus Linnaeus, 1758 (Syn. Tetraodon fahaka) for the first time. Adult A. impletum have a markedly large, sub-terminal oral sucker and a small ventral sucker. As with most trematodes, tegumental spines are concentrated anteriorly and are absent just anterior the ventral sucker. Spines have serrated tips on a short, tongue–shaped body. At the level of the ventral sucker the base of each spine exhibits a three bulbous-like structure that can be partially or completely withdrawn into the tegument. Sensory papillae are concentrated around the oral and ventral suckers and genital pores. Papillae are conical or knob-like, either ciliated or non-ciliated; some are protruded and others are embedded inside the tegument. In the juvenile stage, spines are smaller, less well-developed and tightly packed. The cytoplasmic processes of the posterior quarter of body show brain-like velvety appearance on the adult and small cobblestone-like on the juvenile.

Keywords

Introduction

The trematode, Astiotrema impletum (Looss, 1899) Looss 1900 was first described from the fresh and brackish water globe fish, Tetraodon lineatus Linnaeus, 1758. It has also been reported from the same host species in Egypt and Sudan (Odhner, 1911; Sheng-Liang & Fotedar, 1958; Fischthal & Kuntz, 1963; Khalil, 1969). Yamaguti (1958) considered T. lineatus as the type host of A. impletum. The majority of the studies provided a detailed morphological description of the adult A. impletum through light microscopy and have revealed a significantly larger oral sucker than ventral sucker (Bray et al., 2006; Sheng-Liang & Fotedar, 1958; Siddiqui, 1958; Khalil, 1959; Fischthal & Kuntz, 1963; Siddiqi 1965). In Egypt, Hamada (2002) described the surface ultrastructure of a trematode, identifi ed as A. impletum from Oreochromis niloticus niloticus (Linnaeus, 1758) but having the ventral sucker larger than the oral sucker. Unfortunately Hamada (2002) did not describe any other morphological features that would allow identifi cation of her Astiotrema sp.. Comparing the trematode described by Hamada (2002) with specimens of the presented study however, clearly shows that two different trematode species, possibly even genera, have been involved (Table 1). Major differences in the spine and papillae distribution patterns between the two trematodes are readily evident, especially around the suckers. Given the confusion of the trematode species in the Hamada (2002) study, the aim of our study is to describes the surface ultrastructure of adult

Significant differences between Astiotrema impletum described in this study and the trematode recorded by Hamada (2002).

Feature Present Study Hamada (2002)
Host Fahaka, Nile Pufferfish Tetraodon lineatus Tetraodontiformes Tetradontidae White Tilapia Orechromis niloticus Perciformes Cichlidae
Oral sucker much larger than ventral sucker. yes no
Ventral sucker found in the anterior quarter of the worm. no yes
Ventral sucker surrounded by numerous spines no yes
Ventral sucker with sensory papillae and tend to be in four clusters. yes No, papillae absent.
Tegumental area between the oral and ventral suckers. Square-shaped and has relatively small spines directed posterolaterally and arranged in parallel rows. Rectangular and naked.

and juvenile A. impletum from the type host, T. lineatus. Scanning electron microscopy is now commonly used in studies of digenetic trematodes as it provides valuable data for their identification and characterization of developmental stages (Scholz et al., 1992; Sohn et al., 2003).

Materials and Methods

A total of 40 Nile puffer Tetraodon lineatus were collected by local fisherman between January 2017 and September 2018 from Nile basin and El-Ibrahimia canal next to El-Minia city (28° 04′ − 28° 06′ N and 30° 45′ − 30° 46′ E), Upper Egypt. Fish were taken to the laboratory in a portable aquarium fitted with an air pump. Fish were examined and the recovered adult and juvenile trematodes were placed in 0.75 % physiological saline. After washing in saline, worms were immediately fixed for 2 hours in hot 4% neutral buffered formalin (see de Chambrier et al. (2009)) and then washed in 2.5% glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.2) at 4° C for 2 h. and post fixed for 3 h using 1% osmium tetroxide in the same buffer at 4° C. After washing in buffer, worms were dehydrated in ascending ethanol series and acetone, and dried in a critical-point drying machine using liquid carbon dioxide as a transitional medium. Dehydrated worms were mounted on metallic stubs and coated with gold under vacuum for 10 min. at a setting of 10 – 15 mA using a JEOL JFC-1100E ion sputtering device. Examination was with a JEOL JSM-5400 LV stereo scan device at an acceleration of 15 kV.

For light microscopy, the isolated worms were washed in 0.75% physiological saline solution, fixed in 10% neutral buffered formalin, stained in acetic alum carmine, dehydrated in an ascending series of ethanol, cleared in clove oil, and then mounted in DPX (Morsy et al., 2018). Drawing was made by using a camera Lucida. All measurements were presented in millimeters.

Ethical Approval and/or Informed Consent

Animal care and handling were carried out in accordance with all the relevant national regulations and institutional policies.

Results

Adult worms were bearing egg and varied from 1.7 to 2.63 mm long with mean of 2 mm. Juvenile worms lacked eggs, varied from 1 to 1.5 mm with a mean of 1.19. Other worms in both categories were selected for study with light microscope (Table 2).

Statistical parameters of dimensions and indices of the adult and juvenile Astiotrema impletum (Looss, 1899) Looss 1900 from the Nile puffer fish Tetraodon lineatus Linnaeus, 1758 in Egypt. (Metric characters are in mm.)

Morphological Adult Juvenile
parameters Mean SD n SE Mean SD n SE
Total body length 2 0.3860 8 0.1367 1.19 0.1400 8 0.0574
Maximum width 0.5 0.1455 8 0.0515 0.46 0.0770 8 0.0315
Oral sucker length 0.27 0.0489 8 0.0122 0.24 0.0200 8 0.0083
Oral sucker width 0.34 0.1132 8 0.0128 0.27 0.0340 8 0.0173
Ventral sucker length 0.16 0.0351 8 0.0132 0.15 0.0270 7 0.0097
Ventral sucker width 0.18 0.0348 8 0.0131 0.15 0.0320 7 0.0114
Ant. testis length 0.27 0.0443 8 0.0156 0.13 0.0450 6 0.0183
Ant. testis width 0.23 0.0512 8 0.0181 0.12 0.0400 6 0.0166
Post. testis length 0.34 0.0504 8 0.0178 0.15 0.0640 6 0.0264
Post. testis width 0.27 0.0296 8 0.0104 0.13 0.0650 6 0.0265
Cirrus sac length 0.32 0.0977 7 0.0369 0.12 0.0400 3 0.0233
Ovary length 0.16 0.0349 8 0.0123 - - - -
Ovary width 0.18 0.0370 8 0.0130 - - - -
Egg length 0.040 0.0055 8 0.0021 - - - -
Egg width 0.0124 0.0028 8 0.0012 - - - -
Adult Worm

SEM characterization was based on 10 specimens. The oral and ventral suckers are well-developed; the former is markedly stronger and their relative size ratio is 1.8 – 1, respectively (Fig. 1A). The sub-terminal oral sucker is sub-globular and has no distinct lips. The smaller ventral sucker, however, is nearly rounded and in a median position at the beginning of the second third of the body. The genital opening is slightly sinistral to the midline of the body, just anterior ventral sucker (Fig. 1A).

Fig. 1

Scanning electron micrographs (SEM) of adult Astiotrema impletum.

A – Ventral view of whole body. B – Distribution of sensory papillae around oral sucker and mouth. C – Different shapes of sensory papillae on oral sucker. D – Randomly distributed papillae on naked tegument surrounding ventral sucker. E – Solitary knob-like ciliated papillae and grouped papillae in vicinity of ventral sucker. Abbreviations: ccp – conical ciliated papillae; cnp – conical non-ciliated papillae; ecp – embedded ciliated papillae; enp – embedded non-ciliated papillae; eo – excretory opening; go – genital opening; kcp – knob-like ciliated papillae; mo – mouth opening; os – oral sucker; vs – ventral sucker; arrowheads indicate sensory papillae.

Sensory papillae randomly surround only both suckers and genital opening. Sensory papillae of the oral sucker are numerous and either solitary or in groups of two to eight; they scatter on the lateral sides of the mouth opening close to the corners (Fig. 1B). They show some variation in size and shape, ranging from knob-like to conical; the majority appears to have a single cilium. Some of these papillae are obviously protruded with a cilium, others are embedded inside the tegument (Fig. 1C). Papillae around ventral sucker (Fig. 1D) are smaller and fewer than those of the oral sucker. Most papillae vary in size and are knob-like with short cilia (Fig. 1E). Papillae are slightly smooth and arranged either solitary or clusters of two to five. There are fewer papillae anterior the ventral sucker and around the genital opening.

The dorsal and ventral surface of the anterior part of A. impletum is densely covered with backwardly directed spines. Spines gradually disappear on the posterior quarter of the body. Spines are absent from just anterior the ventral sucker and near the genital opening (Fig. 2A). Ventral spines are closely spaced short, blunt and tongue-shaped with serrated tips (Fig. 2B). Posterior to the ventral sucker, spines increase in length. The base of each spine exhibits three bulbous-like structures (Fig. 2C). The latter are observed sometimes hidden, either partially or completely, inside the tegument. Near the posterior end spines decrease in size and density and have a more corrugated surface (Fig. 2D) before disappearing. The naked posterior quarter and of the body surface has a vermicular or brain-like appearance (Fig. 2E). The shape and distribution of dorsal and ventral spines are similar. The excretory pore is at the posterior extremity, in an indentation and slightly shifted ventrally (Fig. 2F).

Fig. 2

SEM of ventral surface of adult A. impletum.

A – Naked area around and anterior ventral sucker. B – Tegumental spines of anterior ventro -lateral surface of body, just posterior to oral sucker. C – Tegumental spines on the ventro- lateral part, at level of ventral sucker, are long and pointed. D – Tegumental spines on the ventro -lateral part, at level of third quarter of body are smaller, fewer and more corrugated or with parallel surface ridges. E – Cytoplasmic processes on tegument of posterior end have a vermiculate, brain-like velvety appearance. F – Excretory opening is slightly shifted towards ventral surface. Abbreviations: eo – excretory opening; na – naked area in front of ventral sucker; vs – ventral sucker.

Juvenile Stage

SEM characterization was based on 35 specimens. The immature worm generally appears like a smaller adult: dorso-ventrally flattened and blunt at both ends (Fig. 3A). The oral sucker is therefore large, wide, sub-terminal and lacking distinct lips. The ventral sucker, slightly anterior of mid-body, is somewhat rounded and slightly elevated above the body tegument (Fig. 3A). Relative size ratio of oral sucker to ventral one is about 1.7 – 1, respectively. Sensory papillae are few, with same distribution as that of the adult. On the oral sucker, they occur either solitary or in clusters of two to six (Fig. 3B). Few sensory papillae are scattered away from the genital opening. The latter has a position seen in adult worms (Fig. 3C). About 14 variable knob-like sensory papillae in four loose clusters surround the ventral sucker. Some of them have a short cilium (Fig. 3D). The body is covered by smaller backwardly directed spines, with the same distribution seen on adult. Posterior oral sucker, spines are tongue-shaped with broad bases and corrugated surfaces. The tegument at the base of each individual spine protrudes upwards, forming a pocket-like structure that surrounds the root of the spine (Fig. 3E). On both sides of the ventral sucker, the spines are much corrugated and are smaller (Fig. 3F). As in the adult, spines gradually disappear at the posterior extremity. The cytoplasmic processes on the naked posterior part of the body have a fine granulate or small cobblestone-like appearance (Fig. 3G).

Fig. 3

SEM of juvenile Astiotrema impletum.

A – Ventral view of whole body. B – Distribution of sensory papillae on and around oral sucker. C – Genital opening. D - Ventral sucker surrounded by a number of randomly distributed sensory papillae. E – Tegumental spines on anterior ventro -lateral side of body, just posterior to oral sucker. Note pocket-like tegument covering bases of spines. F – Tegumental spines on ventro -lateral surface of body at level of ventral sucker. The spines are small in size and with parallel surface ridges or corrugated. G – Cytoplasmic processes of tegument display a fine granulated or small cobblestone-like appearance on the posterior end of body. Abbreviations: go – genital opening; mo – mouth opening; os – oral sucker; vs – ventral sucker; arrowheads indicate sensory papillae.

Discussion

The genus Astiotrema Looss, 1899 includes about 28 species described from tortoises, snakes and fish in Asia and Africa (Besprozvannykh et al., 2015; Zhokhov et al., 2017). Astiotrema impletum has been previously studied from the fresh water globe fish T. lineatus in Egypt and Sudan using light microscopy (Fischthal & Kuntz, 1963; Khalil, 1969; Mehra, 1931; Odhner, 1911; Sheng-Liang & Fotedar, 1958). Hamada (2002) has done the only surface topography. Lack of data on SEM morphology of most species prevents analysis of systematic relationships within the genus. There have been successive revisions that have evaluated the validity of species resulting in many synonyms (Bhalerao, 1936; Gupta, 1954; Khalil, 1959; Sheng-Liang & Fotedar, 1958; Siddiqi, 1965). Besprozvannykh et al. (2015) discussed the contradictory status of species within the genus Astiotrema. Only A. reniferum (looss, 1898) and A. impletum have been reported from freshwater fish (Agrawal, 1966; Sheng-Liang & Fotedar, 1958; El-Naggar, 1991).

There is a serious question of the correct identity of the trematode studied by Hamada (2002), identified as A. impletum, from Oreochromis n. niloticus. As already noted, Hamada (2002) indicated that her specimens had a ventral sucker significantly larger than the oral sucker. According to Siddiqui (1958), Khalil (1959) and Siddiqi (1965) however, the oral sucker of A. impletum is significantly larger than the ventral one. In addition, her specimens came from tilapia while A. impletum had never been reported from any other fish host except T. lineatus. That fact led Mehra (1931) to concluded that A. impletum is a unique species known only from T. fahaka. (see Scholz et al. (2018)) for history of trematode infections in fish from Egypt). Because of the difference in sucker morphology and the question of host specificity, we consider our study as the first description of the surface topography of A. impletum and its juvenile stage for reasons of morphology and on specimens from the type-host, T. lineatus.

In the present study, SEM analysis showed that the tegument of adult and juvenile A. impletum is covered by spines. This pattern is similar to that of diverse trematodes (Bennett, 1975; El-Naggar et al.,1993b; Ibraheem, 2006; Dumbo et al., 2019): dense anteriorly with gradually decrease in density and size towards the posterior end. Sheng-Liang and Fotedar (1958) had earlier detected dense distribution of spines or cuticular scales on the anterior third of adult A. impletum, and a sparse distribution on the posterior part. Similar observations have been recorded in trematodes such as Fasciola hepatica by Bennett (1975), A. reniferum by El-Naggar et al. (1993b), Orientocreadium batrachoides by El-Naggar et al. (1993a), Acanthostomum spp. by Ibraheem (2006) and Masenia nkomatiensis by Dumbo et al. (2019). Hong et al. (2004) considered reduction of spines on the posterior half of body of Macroorchis spinulosus as an adaptation for increasing absorptive surface area. In the present study, each tegumental spine exhibits a three bulbous-like base, originating from the underlying tegument. In many cases, these structures were partially or completely withdrawn inside the tegument. This suggests to us that individual spines may have, to some extent, ability for functional mobility that may enhance abrasion of intestinal mucosa to produce tissue debris for feeding. On the other hand, they may act as a locomotive apparatus.

The tegument of the present trematode showed a fine granulated or small cobblestone-like appearance on the body surface of the juvenile stage that is gradually differentiated into a velvety, vermiculated appearance on the adult. Similar developmental differentiation has been reported in some other trematodes like Heterophyopsis continua (Hong et al., 1991), Metagonimus miyatai (Chai et al., 1998) and Macroorchis spinulosus (Hong et al., 2004). Gupta et al. (2017) considered the rough, granulated or cobblestone-like processes on the body of Allogenarchopsis bareilliensis as an efficient adaptive feature for increased absorption.

Sensory papillae were detected above the oral sucker, around the ventral sucker and the genital opening of both adults and juveniles. They were more numerous on the adults. Similar observations were detected on Clonorchis sinensi by Fujino et al. (1979) and Himasthla alincia by Han et al. (2003).

Bakke (1976) stated that absence of spines on rim of oral and ventral suckers of Leucochlorodium sp. is necessary for a smooth seal to host’s mucosa.

Fig. 1

Scanning electron micrographs (SEM) of adult Astiotrema impletum.A – Ventral view of whole body. B – Distribution of sensory papillae around oral sucker and mouth. C – Different shapes of sensory papillae on oral sucker. D – Randomly distributed papillae on naked tegument surrounding ventral sucker. E – Solitary knob-like ciliated papillae and grouped papillae in vicinity of ventral sucker. Abbreviations: ccp – conical ciliated papillae; cnp – conical non-ciliated papillae; ecp – embedded ciliated papillae; enp – embedded non-ciliated papillae; eo – excretory opening; go – genital opening; kcp – knob-like ciliated papillae; mo – mouth opening; os – oral sucker; vs – ventral sucker; arrowheads indicate sensory papillae.
Scanning electron micrographs (SEM) of adult Astiotrema impletum.A – Ventral view of whole body. B – Distribution of sensory papillae around oral sucker and mouth. C – Different shapes of sensory papillae on oral sucker. D – Randomly distributed papillae on naked tegument surrounding ventral sucker. E – Solitary knob-like ciliated papillae and grouped papillae in vicinity of ventral sucker. Abbreviations: ccp – conical ciliated papillae; cnp – conical non-ciliated papillae; ecp – embedded ciliated papillae; enp – embedded non-ciliated papillae; eo – excretory opening; go – genital opening; kcp – knob-like ciliated papillae; mo – mouth opening; os – oral sucker; vs – ventral sucker; arrowheads indicate sensory papillae.

Fig. 2

SEM of ventral surface of adult A. impletum.A – Naked area around and anterior ventral sucker. B – Tegumental spines of anterior ventro -lateral surface of body, just posterior to oral sucker. C – Tegumental spines on the ventro- lateral part, at level of ventral sucker, are long and pointed. D – Tegumental spines on the ventro -lateral part, at level of third quarter of body are smaller, fewer and more corrugated or with parallel surface ridges. E – Cytoplasmic processes on tegument of posterior end have a vermiculate, brain-like velvety appearance. F – Excretory opening is slightly shifted towards ventral surface. Abbreviations: eo – excretory opening; na – naked area in front of ventral sucker; vs – ventral sucker.
SEM of ventral surface of adult A. impletum.A – Naked area around and anterior ventral sucker. B – Tegumental spines of anterior ventro -lateral surface of body, just posterior to oral sucker. C – Tegumental spines on the ventro- lateral part, at level of ventral sucker, are long and pointed. D – Tegumental spines on the ventro -lateral part, at level of third quarter of body are smaller, fewer and more corrugated or with parallel surface ridges. E – Cytoplasmic processes on tegument of posterior end have a vermiculate, brain-like velvety appearance. F – Excretory opening is slightly shifted towards ventral surface. Abbreviations: eo – excretory opening; na – naked area in front of ventral sucker; vs – ventral sucker.

Fig. 3

SEM of juvenile Astiotrema impletum.A – Ventral view of whole body. B – Distribution of sensory papillae on and around oral sucker. C – Genital opening. D - Ventral sucker surrounded by a number of randomly distributed sensory papillae. E – Tegumental spines on anterior ventro -lateral side of body, just posterior to oral sucker. Note pocket-like tegument covering bases of spines. F – Tegumental spines on ventro -lateral surface of body at level of ventral sucker. The spines are small in size and with parallel surface ridges or corrugated. G – Cytoplasmic processes of tegument display a fine granulated or small cobblestone-like appearance on the posterior end of body. Abbreviations: go – genital opening; mo – mouth opening; os – oral sucker; vs – ventral sucker; arrowheads indicate sensory papillae.
SEM of juvenile Astiotrema impletum.A – Ventral view of whole body. B – Distribution of sensory papillae on and around oral sucker. C – Genital opening. D - Ventral sucker surrounded by a number of randomly distributed sensory papillae. E – Tegumental spines on anterior ventro -lateral side of body, just posterior to oral sucker. Note pocket-like tegument covering bases of spines. F – Tegumental spines on ventro -lateral surface of body at level of ventral sucker. The spines are small in size and with parallel surface ridges or corrugated. G – Cytoplasmic processes of tegument display a fine granulated or small cobblestone-like appearance on the posterior end of body. Abbreviations: go – genital opening; mo – mouth opening; os – oral sucker; vs – ventral sucker; arrowheads indicate sensory papillae.

Statistical parameters of dimensions and indices of the adult and juvenile Astiotrema impletum (Looss, 1899) Looss 1900 from the Nile puffer fish Tetraodon lineatus Linnaeus, 1758 in Egypt. (Metric characters are in mm.)

Morphological Adult Juvenile
parameters Mean SD n SE Mean SD n SE
Total body length 2 0.3860 8 0.1367 1.19 0.1400 8 0.0574
Maximum width 0.5 0.1455 8 0.0515 0.46 0.0770 8 0.0315
Oral sucker length 0.27 0.0489 8 0.0122 0.24 0.0200 8 0.0083
Oral sucker width 0.34 0.1132 8 0.0128 0.27 0.0340 8 0.0173
Ventral sucker length 0.16 0.0351 8 0.0132 0.15 0.0270 7 0.0097
Ventral sucker width 0.18 0.0348 8 0.0131 0.15 0.0320 7 0.0114
Ant. testis length 0.27 0.0443 8 0.0156 0.13 0.0450 6 0.0183
Ant. testis width 0.23 0.0512 8 0.0181 0.12 0.0400 6 0.0166
Post. testis length 0.34 0.0504 8 0.0178 0.15 0.0640 6 0.0264
Post. testis width 0.27 0.0296 8 0.0104 0.13 0.0650 6 0.0265
Cirrus sac length 0.32 0.0977 7 0.0369 0.12 0.0400 3 0.0233
Ovary length 0.16 0.0349 8 0.0123 - - - -
Ovary width 0.18 0.0370 8 0.0130 - - - -
Egg length 0.040 0.0055 8 0.0021 - - - -
Egg width 0.0124 0.0028 8 0.0012 - - - -

Significant differences between Astiotrema impletum described in this study and the trematode recorded by Hamada (2002).

Feature Present Study Hamada (2002)
Host Fahaka, Nile Pufferfish Tetraodon lineatus Tetraodontiformes Tetradontidae White Tilapia Orechromis niloticus Perciformes Cichlidae
Oral sucker much larger than ventral sucker. yes no
Ventral sucker found in the anterior quarter of the worm. no yes
Ventral sucker surrounded by numerous spines no yes
Ventral sucker with sensory papillae and tend to be in four clusters. yes No, papillae absent.
Tegumental area between the oral and ventral suckers. Square-shaped and has relatively small spines directed posterolaterally and arranged in parallel rows. Rectangular and naked.

AGRAWAL, V. (1966): Four trematode parasites (Plagiorchiidae Lühe, 1901 emend. Ward, 1917) from reptiles of Lucknow. Rev. Biol. Trop., 14(2): 133–151AGRAWAL V. 1966 Four trematode parasites (Plagiorchiidae Lühe, 1901 emend Ward, 1917) from reptiles of Lucknow. Rev. Biol. Trop. 14 2 133 151Search in Google Scholar

BAKKE, T.A. (1976): Functional morphology and surface topography of Leucochloridium sp.(Digenea), revealed by scanning electron microscopy. Z Parasitenkd., 51(1): 115–128BAKKE T.A. 1976 Functional morphology and surface topography of Leucochloridium sp.(Digenea), revealed by scanning electron microscopy Z Parasitenkd. 51 1 115 128Search in Google Scholar

BENNETT, C.E. (1975): Scanning electron microscopy of Fasciola hepatica L. during growth and maturation in the mouse. J Parasitol., 61(5): 892–898. DOI: 10.2307/3279230BENNETT C.E. 1975 Scanning electron microscopy of Fasciola hepatica L during growth and maturation in the mouse. J Parasitol. 61 5 892 898 10.2307/3279230Open DOISearch in Google Scholar

BESPROZVANNYKH, V.V., ATOPKIN, D.M., ERMOLENKO, A.V., KHARITONOVA, A.V., KHAMAT OVA, A.Y. (2015): Life-cycle and genetic characterization of Astiotrema odhneri Bhalerao, 1936 sensu Cho & Seo 1977 from the Primorsky Region (Russian Far East). Parasitol. Int., 64(6): 533–539. DOI: 10.1016/j.parint.2015.07.008BESPROZVANNYKH V.V. ATOPKIN D.M. ERMOLENKO A.V. KHARITONOVA A.V. KHAMAT OVA A.Y. 2015 Life-cycle and genetic characterization of Astiotrema odhneri Bhalerao, 1936 sensu Cho & Seo 1977 from the Primorsky Region (Russian Far East) Parasitol. Int. 64 6 533 539 10.1016/j.parint.2015.07.008Open DOISearch in Google Scholar

BHALERAO, G. (1936): Studies on the helminths of India. Trematoda II. J. Helminthol., 14(4):181–206BHALERAO G. 1936 Studies on the helminths of India Trematoda II. J. Helminthol. 14 4 181 206Search in Google Scholar

BRAY, R.A., VAN OOSTERHOUT, C., BLAIS, J., CABLE, J. (2006): Astiotrema turneri n. sp (Digenea: Plagiorchiidae) from cichlid fishes (Cichlidae: Perciformes) of Lake Malawi, south-eastern Africa. Zootaxa, 1319(1), 43–58. DOI: 10.11646/zootaxa.1319.1.4BRAY R.A. VAN OOSTERHOUT C. BLAIS J. CABLE J. 2006 Astiotrema turneri n sp (Digenea: Plagiorchiidae) from cichlid fishes (Cichlidae: Perciformes) of Lake Malawi, south-eastern Africa. Zootaxa 1319 1 43 58 10.11646/zootaxa.1319.1.4Open DOISearch in Google Scholar

CHAI, J.Y., KANG, Y.J., CHOI, S.Y., GUK, S.M., YU, J.R., LEE, S.H. (1998): Surface ultrastructure of Metagonimus miyatai metacercariae and adults. Korean J. Parasitol., 36(4): 217–225. DOI: 10.3347/kjp.1998.36.4.217CHAI J.Y. KANG Y.J. CHOI S.Y. GUK S.M. YU J.R. LEE S.H. 1998 Surface ultrastructure of Metagonimus miyatai metacercariae and adults Korean J. Parasitol. 36 4 217 225 10.3347/kjp.1998.36.4.217Open DOISearch in Google Scholar

DE CHAMBRIER, A., SCHOLZ, T., BELETEW, M., MARIAUX, J. (2009): A new genus and species of proteocephalidean (Cestoda) from Clarias catfishes (Siluriformes: Clariidae) in Africa. J. Parasitol., 95(1): 160–168. DOI: 10.1645/GE-1594.1DE CHAMBRIER A. SCHOLZ T. BELETEW M. MARIAUX J. 2009 A new genus and species of proteocephalidean (Cestoda) from Clarias catfishes (Siluriformes: Clariidae) in Africa J. Parasitol. 95 1 160 168 10.1645/GE-1594.1Open DOISearch in Google Scholar

DUMBO, J.C., DOS SANTOS Q.M., AVENANT-OLDEWAGE, A. (2019): Masenia nkomatiensis n. sp.(Digenea: Cephalogonimidae) from Clarias gariepinus (Burchell)(Clariidae) in Incomati Basin, Mozambique. Syst. Parasitol., 96(3): 311–326. DOI: 10.1007/s11230019-09848-w EL-NAGGAR, M. (1991): Redescription of Astiotrema reniferumDUMBO J.C. DOS SANTOS Q.M. AVENANT-OLDEWAGE A. 2019 Masenia nkomatiensis n sp.(Digenea: Cephalogonimidae) from Clarias gariepinus (Burchell)(Clariidae) in Incomati Basin, Mozambique. Syst. Parasitol. 96 3 311 326 10.1007/s11230019-09848-w EL-NAGGAR, M. (1991): Redescription of Astiotrema reniferumOpen DOISearch in Google Scholar

(Looss, 1898) Stossich 1904, a digenean intestinal parasite of Clarias lazera in Egypt. Japanese J. Parasitol., 40(3): 245–252(Looss, 1898) Stossich 1904, a digenean intestinal parasite of Clarias lazera in Egypt Japanese J. Parasitol. 40 3 245 252Search in Google Scholar

EL-NAGGAR, M., IBRAHIM, H., HAMADA, S. (1993a): Scanning andtransmission electron microscope observations on the general body tegument and ventral pads of the digenean Orientocreadium batrachoides Tubangui, 1931. J. Egyptian-German Soc. Zool., Invertebrate zoology & parasitology, 10: 245–264EL-NAGGAR M. IBRAHIM H. HAMADA S. 1993a Scanning andtransmission electron microscope observations on the general body tegument and ventral pads of the digenean Orientocreadium batrachoides Tubangui, 1931 J. Egyptian-German Soc. Zool., Invertebrate zoology & parasitology 10 245 264Search in Google Scholar

EL-NAGGAR, M.M., IBRAHIM, H.A., HAMADA, S.F. (1993b): Scanning electron microscope observations on the digenean intestinal parasite Astiotrema reniferum (Plagiorchiidae). J Egypt Soc. Parasitol., 23(1): 141–150EL-NAGGAR M.M. IBRAHIM H.A. HAMADA S.F. 1993b Scanning electron microscope observations on the digenean intestinal parasite Astiotrema reniferum (Plagiorchiidae) J Egypt Soc. Parasitol. 23 1 141 150Search in Google Scholar

FISCHTHAL, J.H., KUNTZ, R.E. (1963): Trematode parasites of fishes from Egypt. Part V. Annotated record of some previously described forms. J. Parasitol., 49(1): 91–98FISCHTHAL J.H. KUNTZ R.E. 1963 Trematode parasites of fishes from Egypt Part V. Annotated record of some previously described forms. J. Parasitol. 49 1 91 98Search in Google Scholar

FUJINO, T., ISHII, Y., CHOI, D.W. (1979): Surface ultrastructure of the tegument of Clonorchis sinensis newly excysted juveniles and adult worms. J. Parasitol., 65(4): 579–590. DOI: 10.2307/3280325 GUPTA, N. (1954): On five new trematodes of the genus Astiotrema Looss, 1900, from the intestine of Lissemys punctata punctata and discussion on the synonymity of two already known forms. Res. Bulletin Panjab Univ., (49/50): 85–100 FUJINO T. ISHII Y. CHOI D.W. 1979 Surface ultrastructure of the tegument of Clonorchis sinensis newly excysted juveniles and adult worms J. Parasitol. 65 4 579 590 10.2307/3280325 GUPTA, N. (1954): On five new trematodes of the genus Astiotrema Looss, 1900, from the intestine of Lissemys punctata punctata and discussion on the synonymity of two already known forms. Res. Bulletin Panjab Univ., (49/50): 85–100Open DOISearch in Google Scholar

GUPTA, N., GUPTA, D.K., URABE, M. (2017): Taxonomic tools for the identification of Allogenarchopsis bareilliensis n. sp.(Digenea: Hemiuroidea: Derogenidae) from Channastriata of Rohilkhand, India based on light and scanning electron microscopic studies. J. parasit. dis., 41(1): 29–39GUPTA N. GUPTA D.K. URABE M. 2017 Taxonomic tools for the identification of Allogenarchopsis bareilliensis n sp.(Digenea: Hemiuroidea: Derogenidae) from Channastriata of Rohilkhand, India based on light and scanning electron microscopic studies. J. parasit. dis. 41 1 29 39Search in Google Scholar

HAMADA, S.F. (2002): Scanning electron microscope observations of the surface features of the digenean Astiotrema impletum (Looss, 1899) Looss 1900. J. Egypt Soc. Parasitol., 32(2): 487–500HAMADA S.F. 2002 Scanning electron microscope observations of the surface features of the digenean Astiotrema impletum (Looss, 1899) Looss 1900 J. Egypt Soc. Parasitol. 32 2 487 500Search in Google Scholar

HAN, E.T., HAN, K.Y., CHAI, J.Y. (2003): Tegumental ultrastructure of the juvenile and adult Himasthla alincia (Digenea: Echinostomatidae). Korean J. Parasitol., 41(1): 17–25. DOI: 10.3347/kjp.2003.41.1.17HAN E.T. HAN K.Y. CHAI J.Y. 2003 Tegumental ultrastructure of the juvenile and adult Himasthla alincia (Digenea: Echinostomatidae) Korean J. Parasitol. 41 1 17 25 10.3347/kjp.2003.41.1.17Open DOISearch in Google Scholar

HONG, S.J., CHAI, J.Y., LEE, S.H. (1991): Surface ultrastructure of the developmental stages of Heterophyopsis continua (Trematoda: Heterophyidae). J. Parasitol., 77(4): 613–620HONG S.J. CHAI J.Y. LEE S.H. 1991 Surface ultrastructure of the developmental stages of Heterophyopsis continua (Trematoda: Heterophyidae) J. Parasitol. 77 4 613 620Search in Google Scholar

HONG, S.J., WOO, H.C., KWON, O.S. (2004): Developmental surface ultrastructure of Macroorchis spinulosus in albino rats. Korean J. Parasitol., 42(4): 151–157. DOI: 10.3347/kjp.2004.42.4.151 IBRAHEEM, M.H. (2006): On the morphology of Acanthostomum spiniceps (Looss, 1896) and A. absconditum (Looss, 1901) (Digenea: Cryptogonimidae: Acanthostominae) with particular reference to the juvenile stage. Acta Zoologica, 87(3): 159–169. DOI: 10.1111/j.1463-6395.2006.00227.xHONG S.J. WOO H.C. KWON O.S. 2004 Developmental surface ultrastructure of Macroorchis spinulosus in albino rats Korean J. Parasitol. 42 4 151 157 10.3347/kjp.2004.42.4.151 IBRAHEEM, M.H. (2006): On the morphology of Acanthostomum spiniceps (Looss, 1896) and A. absconditum (Looss, 1901) (Digenea: Cryptogonimidae: Acanthostominae) with particular reference to the juvenile stage. Acta Zoologica, 87(3): 159–169. 10.1111/j.1463-6395.2006.00227.xOpen DOISearch in Google Scholar

KHALIL, L.F. (1959): On a new trematode, Astiotrema sudanensis, sp. nov., from a freshwater turtle in the Sudan. J. Helminthol., 33(4): 263–266. DOI: 10.1017/s0022149x00020149KHALIL L.F. 1959 On a new trematode, Astiotrema sudanensis, sp nov., from a freshwater turtle in the Sudan. J. Helminthol. 33 4 263 266 10.1017/s0022149x00020149Open DOISearch in Google Scholar

KHALIL, L.F. (1969). Studies on the helminth parasites of freshwater fishes of the Sudan. J. Zool., 158(2): 143–170. DOI: 10.1111/j.1469-7998.1969.tb02132.xKHALIL L.F. 1969 Studies on the helminth parasites of freshwater fishes of the Sudan J. Zool. 158 2 143 170 10.1111/j.1469-7998.1969.tb02132.xOpen DOISearch in Google Scholar

MEHRA, H. (1931): On two new species of the genus Astiotrema Looss belonging to the family Lepodermatidae Odhner. Parasitology, 23(2): 179–190MEHRA H. 1931 On two new species of the genus Astiotrema Looss belonging to the family Lepodermatidae Odhner Parasitology 23 2 179 190Search in Google Scholar

MORSY, K., ABDEL-GHAFFA R, F., BASHTAR, A.R., DAJEM, S.B., ABDEL-GABER, R., MOSTAFA, M. (2018): Light microscopy and surface topography of Urotrema scabridum and Renschetrema indicum (Digenea) from Rhinopoma hardwickii (Chiroptera): first report in Egypt. Rev. Bras. Parasitol. Vet., 27(3): 319–326. DOI: 10.1590/S1984-296120180039MORSY K. ABDEL-GHAFFA R F. BASHTAR A.R. DAJEM S.B. ABDEL-GABER R. MOSTAFA M. 2018 Light microscopy and surface topography of Urotrema scabridum and Renschetrema indicum (Digenea) from Rhinopoma hardwickii (Chiroptera): first report in Egypt Rev. Bras. Parasitol. Vet. 27 3 319 326 10.1590/S1984-296120180039Open DOISearch in Google Scholar

ODHNER, T. (1911): Nordostafrikanische Trematoden grösstenteils von Weissen Nil. [Northeast African trematodes mostly from white Nile.] Zool. Exp. Egypt and White Nile. IV, 170 pp (In German).ODHNER T. 1911 Nordostafrikanische Trematoden grösstenteils von Weissen Nil. [Northeast African trematodes mostly from white Nile.] Zool. Exp. Egypt and White Nile. IV 170 pp (In German)Search in Google Scholar

SCHOLZ, T., DITRICH, O., GIBODA, M. (1992): Study on the surface morphology of the developmental stages of the liver fluke, Opisthorchis viverrini (Trematoda: Opisthorchiidae). Ann. Parasitol.SCHOLZ T. DITRICH O. GIBODA M. 1992 Study on the surface morphology of the developmental stages of the liver fluke, Opisthorchis viverrini (Trematoda: Opisthorchiidae) Ann. Parasitol.Search in Google Scholar

Hum. Comp., 67(3): 82–90. DOI: 10.1051/parasite/199267382 SCHOLZ, T., VANHOVE, M.P., SMIT, N., JAYASUNDERA, Z., GELNAR, M. (2018). A guide to the parasites of African freshwater fishes. Abc-Taxa, Vol. 18, 425 pp.Hum. Comp. 67 3 82 90 10.1051/parasite/199267382 SCHOLZ, T., VANHOVE, M.P., SMIT, N., JAYASUNDERA, Z., GELNAR, M. 2018: A guide to the parasites of African freshwater fishes. Abc-Taxa, Vol. 18, 425 ppOpen DOISearch in Google Scholar

SHENG-LIANG, Y., FOTEDAR, D. (1958): A review of the trematode genus Astiotrema in the family Plagiorchiidae. J. Helminthol., 32(12): 17–32SHENG-LIANG Y. FOTEDAR D. 1958 A review of the trematode genus Astiotrema in the family Plagiorchiidae J. Helminthol. 32 12 17 32Search in Google Scholar

SIDIQI, A.H. (1965): A new species of the genus Astiotrema Looss, 1900 with a key to its species. J. Helminthol., 39(1): 113–116. SIDIQUI, W.A. (1958): On a new trematode, Astiotrema geomydia (family Plagiorchidae), from an Indian tortoise. Z. Parasitenkd., 18(3): 219–222. DOI: 10.1007/bf00259194SIDIQI A.H. 1965 A new species of the genus Astiotrema Looss, 1900 with a key to its species J. Helminthol. 39 1 113 116 SIDIQUI, W.A. (1958): On a new trematode, Astiotrema geomydia (family Plagiorchidae), from an Indian tortoise. Z. Parasitenkd., 18(3): 219–222 10.1007/bf00259194Open DOISearch in Google Scholar

SOHN, W.M., SEO, M., CHAI, J.Y. (2003): Surface ultrastructure of the adult stage of Acanthotrema felis (Trematoda: Heterophyidae). Korean J. Parasitol., 41(2): 107–111. DOI: 10.3347/kjp.2003.41.2.107SOHN W.M. SEO M. CHAI J.Y. 2003 Surface ultrastructure of the adult stage of Acanthotrema felis (Trematoda: Heterophyidae) Korean J. Parasitol. 41 2 107 111 10.3347/kjp.2003.41.2.107Open DOISearch in Google Scholar

YAMAGUTI, S. (1958): Systema Helminthum. Vol. 1. The digenetic Trematodes of Vertebrates – Part I and II.Interscience Publishers, New York, 860 pp.YAMAGUTI S. 1958 Systema Helminthum. Vol. 1. The digenetic Trematodes of Vertebrates – Part I and II Interscience Publishers New York 860 ppSearch in Google Scholar

ZHOKHOV, A., MOROZOVA, D., PUGACHEVA, M. (2017): Trematodes (Plathelminthes) of Clarias gariepinus (Pisces: Clariidae) in Lake Tana, Ethiopia. Inland Water Biol, 10(2): 219–227. DOI: 10.1134/S1995082917020171ZHOKHOV A. MOROZOVA D. PUGACHEVA M. 2017 Trematodes (Plathelminthes) of Clarias gariepinus (Pisces: Clariidae) in Lake Tana, Ethiopia Inland Water Biol 10 2 219 227 10.1134/S1995082917020171Open DOISearch in Google Scholar

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