J. KAU: Mar. Sci., vol.Pseudoplagioporus 12, Special Issue, interruptos pp. 175-188 Durio... (1421 A.H. / 2001 A.D.) 175

Pseudoplagioporus interruptus Durio and Manter, 1968 and agyptia sp. n. (Trematoda: Opecoeliidae) from the Red Sea Fish in Egypt

NAHED EL. Abdou,*RICHARD A. HECKMANN, SAMIR M. BELTAGY and **AMEEN A. ASHOUR Department of Biology, Faculty of Education, Ain Shams University, Cairo, *Department of Zoology, WIDB, Brigham Young University, Provo, UT. USA; and **Department of Zoology, Faculty of Science, Ain Shams University, Cairo, Egypt

ABSTRACT. The present investigation includes a description of two species of trema- todes, Hamacreadium egyptia sp. n. and Pseudoplagioporus interruptus Durio and Manter, infecting two fish species, Forsskål, 1775 and L. mahse- na Forsskål, 1775 (Family: ) in the Red Sea. Both trematodes were de- scribed from Egypt for the first time. Fish samples were collected during the period from February to November, 1993. A total of 103 Lethrinidae fishes were examined, the rate of infection was 25%. In Lethrinus nebulosus, 24% were found infected, with the highest prevalence during summer (28%). In case of L. mahsena, 32% were found infected with the highest infection rate during spring (58%). A full description is giv- en to the trematodes using both light and scanning electron microscopy.

KEY WORDS: Helminth parasites, Digenetic trematodes, Ultrastructure, Helminth Preva- lence, Red Sea.

Introduction In Egypt the first record of Pseudoplagioporus nebulosae (Nagaty and Abdel Aal, 1969) was from The Pseudoplagioporus was created by Ya- Lethrinus nebulosus in the Red Sea. Moreover, two maguti (1938) who reported the following morpho- other species of Pseudoplagioporus ''P. microchis logical characters of this genus: This group of Yamaguti 1942 and P. yamagutii Ramadan (1979)'' trematode has a submedian ovary, lying between were also recorded from the Red Sea fishes L. hae- the two testes; occasionally opposite to the anterior matoperus; L. mehsena, L. nebulosus; L. sp.; Mal- testis. Oral sucker and pharynx are well developed. las sp. and Serranus sp., by Ramadan (1979). Genital pore lies sinistral to pharynx or oesopha- gus and vitellaria extend in lateral fields in the Linton established the genus Hamacreadium in bifurco-acetabular zone. The type species of this 1910 for trematodes having oblique testes, preace- genus is Pseudoplagioporus lethrini Yamaguti tabular cirrus pouch, lobulated ovary and caeca ter- (1938) infecting the fish Lethrinus haematopterus minating at the posterior end of the body. He de- from the Pacific coast of Japan and Naha region in scribed H. mutabile from Neomaenis grisens and Ryukyu island. N. apodus (cited in Ramadan, 1983).

175 176 N.E. Abdou et al.

Hamacreadium diacopac (Nagati et al., 1962) Results and Discussion from Diacope falviflama and H. khalili (Ramadan, Pseudoplagioporus interruptus Durio and Mant- 1983) from and L. nebulosus er, 1968 are two other species of Hamacreadium described from Red Sea fishes. Five worms, were collected from the alimentary tracts of fish Lethrinus nebulosus (Forsskål, 1775) Materials and Methods and Lethrinus mahsena (Forsskål, 1775). All measurements in mm. Specimens collected for the present study were purchased from fishermen working in the area of Description Hurghada City. Samples were obtained during 4 visits to the area. Each visit took 4 weeks and the Light microscopy: The trematode worms are schedule was arranged to consider different sea- orange in colour, elongated in shape and range sonal changes over the year (1993) and the time of from 6.0 to 7.0 (6.5) long by 1.3 to 1.5 (1.4) wide. maximal fishing activity. Both ends of the trematode are rounded with slight- ly notched posterior border. All collected samples were taken immediately to the Gohar Laboratory in the same city for study. Rounded Oral sucker is lying subterminal, and Fishs were identified, weighed, measured and measuring 0.24 to 0.32 (0.27) in length by 0.26 to sexed after dissection 0.39 (0.33) in width. The ventral sucker is located at the end of the first third of the body, measuring For Light Microscopy: The parasites were put 0.45 to 0.62 (0.55) in length and 0.39 to 0.68 (0.53) in between two glass slides with a drop of 70% al- in width; numerous characteristic muscle fibers are cohol until they relaxed. After washing with dis- present on both sides of the ventral sucker (Plate 1, tilled water, each specimen was stained in aceto- Fig. 1)Æ They are organized in a radial shape. carmine for 15 min, differentiated in 70% acid- alcohol, dehydrated, and cleaned in clove oil. Pharynx is well developed and followed by a Specimens were mounted on glass slides in Cana- long oesophagus. Intestinal arch is wide and intes- da balsam, covered with thin cover slips and dried tinal caeca are unequal in length. One of the two in an oven at 40ºC. Specimens were drawn by intestinal caeca ends close to the excretory pore, using camera lucida. All measurements were pre- while the other branch is shorter and ends 0.2 from sented in millimeters (mm). the excretory pore. For scanning electron microscopy, another Genitalia composed of 2 diagonal Testes with ir- group of parasites were washed in 0.7% saline so- regular outlines situated intercecal nearly at the lution and fixed in 7% formalin until transferred to middle of the fluke. Their lengths range from 0.27 the Electron Microscope laboratory of Brigham to 0.50 (0.41) and 0.22 to 0.42 (0.37) in width. The Young University, Provo-Utah. In the laboratory, Cirrus sac appears swollen posteriorly and gets each specimen was washed 6 times with sodium narrower anteriorly and terminates in the genital cacodylate buffer (pH 7.2), then fixed in osmium pore. Genital pore is located on the left side just behind the intestinal bifurcation. tetroxide (OsO4) for 2 hr. The fixed samples were washed in buffer solution, then fixed again in Ovary is lobulated, intercecal, lying in the mid- OsO4 for 12 hr. Re-washing in a solution of cacod- dle of the body. Ovary ranges in length from 0.19 ylate buffer was then done, and immersion of sam- to 0.25 (0.23) and 0.28 to 0.32 (30) in width. Vitel- ples into 2% tannic acid for 8 hr was ensued (Mu- line glands are numerous and extend in two groups rakami, 1977). Before the final step of fixation in on both lateral sides of the fluke, at the level just OsO4 for 2 hr, samples were washed in cacodylate posterior to the testes, the vitelline glands appear as buffer again. The samples were dehydrated in a extra – and interacecal bands on both sides of the graded series of ethanol, critical point dried, body, with few of such glands overlap the intesti- mounted on stubs and coated with gold. The sam- nal caeca. The vitelline glands extend anteriorly to ples were observed with a high resolution scanning the level of intestinal bifurcation and posteriorly to electron microscope (Joel 6100). the posterior extremity of the fluke. Each vitelline Pseudoplagioporus interruptos Durio... 177

Plates (1 and 2) Pseudoplagioporus interruptus Durio and Manter, 1968. Plate (1): Fig. 1-2. Light microscopy:

FIG. 1. Light microscope drawing of the fluke showing oral sucker S, pharynx G, intestinal secum n, ventral sucker V, radial muscles F, testes T, ovary O, vitelline glands Vg, egg E, genital pore R, and excretory pore ExÆ FIG. 2. Light microscope image of the fluke. Plate (1): Fig. 3-6. Scanning electron microscope images:

FIG. 3. Whole body of the fluke. Oral sucker O, ventral sucker V, and excretory pore ExÆ FIG. 4. High magnification image of oral sucker showing the distribution of papillae on the tegument of the lip and around the sucker. FIG. 5. High magnification of the square area in Plate 4 showing the tegumental papillae P. FIG. 6. Transverse section of the fluke through the uterus showing eggs EÆ 178 N.E. Abdou et al. gland is oval to elongate in shape and their sizes Scanning electron microscopy: A scanning elec- range from 0.07 to 0.09 (0.07) in length and 0.05 to tron microscopy of the tegument revealed that sur- 0.07 (0.06) in width. Two narrow longitudinal vi- face of the fluke is covered with a rather smooth, telline ducts extend on both sides of the intestinal unarmed tegument. The genital pore is situated at caeca and another middle transverse vitelline duct the mid-distance between the oral and ventral suck- ers. In a transverse section of the fluke at the level is clearly visible (Plate 2 Fig. 1 and 2). of the uterus (Plate 1 Fig. 3). In all cases, Eggs are numerous, fill the uterus, On and around the oral sucker the tegument has which extend anteriorly from the middle vitelline numerous large papillae which have no special ar- duct to the level of ventral sucker. Groups of egg rangement (Plate 1 Fig. 4). At high magnification, measuring 0.06 to 0.08 (0.07) in length and 0.04 in these papillae appear lobulated and measuring 10 width (Plate 1 Fig. 1 and 2). to 15 µm in width (Plate 1 Fig. 5). The tegument of

Plate (2) Scanning Electron Microscope Images (continued).

FIG. 7. High magnification of the body tegument showing the presence of pores (arrows). FIG. 8. High magnification of the surface of the ventral sucker showing Cobblestone-like processes. Pseudoplagioporus interruptos Durio... 179 the ventral sucker reveals cobblestone-like cyto- The present fluke appears different from P. in- plasmic processes (Plate 2 Fig. 8). On the dorsal terruptus, which had been redescribed by Grabda- surface of the fluke, minute pits are found scat- Kazubska (1980) from fish Grenidens indicus in tered in a regular pattern (Plate 2 Fig. 7). Eggs ap- Pakistan, in the position of the ventral sucker and pear smooth, and rounded (Plate 2 Fig. 6). testes. The caecal arch is wider in the present sam- ple compared to the other descriptions of P. inter- Prevalence of Pseudoplagioporus interruptus ruptus of Grabda-KazubskaÆ Durio and Manter, 1968 Pseudoplagioporus inter- ruptus flukes were recovered from Lethrinus nobu- Again, the present specimen can be differentiat- losus and L. mahsena. Among 45 fish belonging to ed from P. interruptus, described from L. chrysos- Lethrinus nebulosus, 11 were found infected with a tomus by Bray and Cribb (1989), in size and posi- percentage of 24%. While in L. mahsena, 16 fishes tion of ventral sucker; body length; and ovary out of 58 examined samples were found infected width. (27%). Table 1 summarizes the prevalence of Pseu- Table 2 shows a comparison between the origi- doplagioporus interruptus in Red Sea fishes. nal description of P. interruptus as given by Durio and Manter (1968), its redescription by Bray and Discussion Cribb (1989), and the present material. The present work represents the first record of According to the available literature no similar P. interruptus Durio and Manter, 1968 from the flukes have been previously studied by the Scan- Red Sea fishes and from the hosts L. nebulosus ning Electron Microscope (SEM). The present and L. mehsenaÆ work may represent the first description of the teg- The obtained sample of Pseudoplagioporus in- umental topography of a member of this family. terruptus, differs from the original description giv- The topographical surface of P. interruptus is en by Durio and Manter (1968). The body appears characterized by, aspinous tegument, few tegumen- longer (Table 2), the extension of vitelline glands tal folds appear around the oral sucker, lobulated was interrupted in the level of testes, while it lies papillae are found on the rim and around the oral opposite to the ventral sucker in the original de- sucker, Cobblestone-like cytoplasmic processes are scription. The position of the genital pore was near found on the rim of the ventral sucker. Absence of to the caecal bifurcation in the present specimen papillae from the ventral and dorsal surface, and however, it is external to the intestinal caeca in the presence of pits on the dorsal surface are character- original description. istic.

TABLE 1. Prevalence of Pseudoplagioporus interruptus Durio and Manter, 1968 in the Red Sea fishes.

Hosts Sex Infection Number Weight range (g) Length range (mm) Spring Summer Fall Winter

Lethrinus nebulosus male inf 8 320 - 1500 32 - 42 1 3 4 0

non 30 155 - 2020 28 - 59 5 10 15 0

female inf 3 685 - 1500 39 - 55 0 1 2 0

non 4 695 - 3100 36 - 60 0 0 4 0

Total 45 155 - 3100 28 - 60 6 14 25 0

Lethrinus mahsena male inf 15 330 - 1240 27 - 42 6 4 5 0

non 37 85 - 1220 19 - 40 4 15 11 7

female inf 1 250 25 1 0 0 0

non 5 270 - 1310 27 - 42 1 2 0 2

Total 58 85 - 1310 19 - 42 12 21 16 9 180 N.E. Abdou et al.

TABLE 2. A comparison of the descriptions of Pseudoplagioporus interruptus by Durio and Manter (1968), Bray and Cribb (1989), and the present.

Pseudoplagioporus Pseudoplagioporus Characters interruptos Durio and Manter, interruptos, Durio and Manter, Present description 1968 1968; Bray and Cribb, 1968 Body: length (mm) 2.2 - 4.3 1.8 - 2.6 4.8 - 5.2 width (mm) 0.72 - 1.33 0.65 - 0.94 1.26 - 1.51 Oral sucker: length (mm) 0.30 - 0.40 0.22 - 0.30 0.24 - 0.32 width (mm) – 0.24 - 0.30 0.26 - 0.39 Ventral sucker: length (mm) 0.47 - 0.71 0.34 - 0.49 0.45 - 0.62 width (mm) – 0.44 - 0.60 0.39 - 0.68 Testes: – in the anterior half separated in the posterior half, in the posterior half by the uterus length (mm) – 0.15 - 0.33 0.27 - 0.50 width (mm) – 0.18 - 0.25 0.22 - 0.42 Ovary: length (mm) – 0.14 - 0.20 0.19 - 0.25 width (mm) – 0.12 - 0.17 0.28 - 0.32 Vitelline glands distribution mid-oesophagus level, interrupted at the level of interrupted at the level of interrupted opposite to the acetabulum and extend to the the testes and extend to the ventral sucker mid pharynx anteriorly mid pharynx anteriorly Egg: length (mm) 51 - 67 µm 51 - 0 µm 62 - 77 µm width (mm) 40 - 59 µm 38 - 59 µm 40 µm Hosts L. sp., L. glyphodon, L. sp., L. chrysostomus, and L. nebulosus and Plectorhynchus sp., L. glyphodon L. mehsena Epinephelus merra and Choerodon albigena Location New Caledonia, Australia New Caledonia, Australia Red Sea, Harghada, Egypt

Aspinous surface of the described trematode Nollen, 1975); Leucochloridium sp. (Bakke, 1976); was previously reported in other flukes such as Concinnum epomopis (Otubanjo, 1985) and Phyllo- Gorgoderina attenuata (Nadakavukaren and Nol- distomum umblae (Bakke and Bailey, 1987). len, 1975); Leucochloridium sp. (Bakke, 1976); The presence of folds on the tegument overlying Phyllodistomum umblae (Bakke and Baily, 1987); the suckers were previously observed in Leucoch- Concinnum epomopis (Otubanjo, 1985) and Aus- loridium sp. by Bakke (1976). He suggested that trobilhariza variglandis (Barber and Caira, 1995). the folds in the oral sucker may result from body The tegumental microtopography of the oral flexure and movements of the oral sucker itself. But sucker was characterized by lobulated papillae for the best of my knowledge, there are no TEM raised from the folds around the oral sucker. These studies so far had been done to insure this idea. papillae could be similar to what was described be- The protuberances ''Cobblestone-like cytoplas- fore under terms (wart-like cuticular bosses of mic process'' of the ventral sucker were described Schistosoma mansoni (Miller et al., 1972); papilla- in many previous studies (Lee et al., 1984, 1987 like integumental elevations of Diplostomum phox- and Chai et al., 1992). They may serve to increase ini (Erasmus, 1970) and spherical surface eleva- the surface area for absorptive function or to give a tions of Gorgoderina attenuata (Nadakavukaren rough surface to the ventral sucker that could be and Nollen, 1975). useful for attachment of the parasite with the intes- The tegumental folds were previously described tinal villi of the host (Nadakavukaren and Nollen from Gorgoderina attenuata (Nadakavukaren & 1975). Pseudoplagioporus interruptos Durio... 181

No sensory papillae were observed on the sur- Bray and Cribb (1989) recorded P. interruptus face of the body of the present fluke, this comes to Durio and Manter (1968) from Lethrium chrysosto- be similar to Gorgoderina attenuata Æ mus and Hamacreadium mutabile Linton (1910) from Lutjanus amabilis in Heron island and Fair- The tegumental pits or holes that were demon- fax Island in the Southern Great Barrier Reef, strated in the present material were characterized Queensland, Australia. by a rounded outline and regular distribution. Pits are observed from several flukes such as Leucoch- 2 – Hamacreadium egyptia sp. n. loridum sp. (Bakke, 1976), Echinostoma revolu- This trematode was also collected from the in- tum (Smales and Blankespoor, 1984); and Concin- testine of Lethrinus nebulosus (Forsskål, 1775) and num epomopis (Otubanjo, 1985). Bakke (1976) Lethrinus mahsena (Forssål, 1775). All measure- assumed that the function of these pits could be se- ments in mm. cretory, absorptive or sensory. Moreover, Smales and Blankespoor (1984) suggested that the pres- Description ence of such pits on the body surface of Echinosto- Light Microscopy; Body is elongate, measuring ma may have a secretory function only. 1.18 long and 0.52 wide, with the maximum width As regards the prevalence of this trematode in at the level of ventral sucker. Fore body is conical fish hosts, the following data were observed: and hind body is rounded and wide. Oral sucker is terminal, spherical and measuring 0.13 long and – In fish Lethrinus nobulosus, the total infection 0.1 wide. Pharynx is globular and measures 0.17 rate was 24%. The highest rate of infection was re- by 0.13. Oesophagus is wide and short, measuring corded during summer season (28%) followed by 0.09 long and 0.05 wide. The caecal bifurcation is 24% in fall, then 16% in spring. No infection was situated much close to the oral sucker rather than to recorded during winter. The female fishes were the ventral sucker. Caecal arch is quite wide and more infected by P. interruptus compared to males the intestinal caeca are unequal in length and termi- (42% and 21% respectively). nate close to the posterior extremity of the body. – In L. mahsena, the total infection rate was Ventral sucker is large, median and measures 0.2 in diameter. higher than that in L. nebulosus (28%). The infec- tion rates were (58%) in spring, (19%) in summer Two testes are slightly irregular in shape and sit- and (31%) in fall. Infection rate in males is higher uated on the posterior third of the body. They are than females (29% and 17% respectively). unequal in size, the left testis is 0.05 long and 0.06 wide and the right testis is 0.06 in diameter. Cirrus At the global level the distribution of genus sac is well developed, it lies obliquely and extends Pseudoplagioporus in the other areas is limited, posteriorly to the ventral sucker, overlapping the according to the available literatures, many species left cecum. Genital pore is situated anteriorly close of the genus were previously described such as to the caecal bifurcation. Pseudoplagioporus microrchis (1942) from Lethri- Ovary is small, rounded and situated on the nus haematopterus from Naha-Ryukyu island, Ja- right side of the body in front of the posterior testis pan; Pseudoplagioporus trematode genera record- and very close to the ventral sucker. It measures ed from the marine fishes of the Arabian Gulf by 0.04 long by 0.03 wide. Vitelline glands are very Saoud et al. in 1986. Pseudoplagioporus lethrini small, continuous, and extending far to the anterior Yamaguti (1938) parasite of Lethrinus sp. and P. end of the body. Eggs are not visible in the present interruptus Durio and Manter, 1968 collected from preparation. Excretory pore is terminal and seen Lethrinus sp. and L. glyphodon were redescribed on the mid posterior extremity of the fluke (Plate 3 from New Caledonia, Australia by Durio and Fig. 1 and 2). Manter (1968). Bilqees (1980) redescribed Pseu- Scanning Electron Microscopy: The trematode doplagioporus interruptus and P. lethrini from the body has a conical shape, which is pointed anteri- fish Crenidens indicus in Karachi coast, Pakistan. orly and has a wide posterior extremity. The excre- 182 N.E. Abdou et al.

Plates (3 and 4) Hamacredium egyptia sp.n. Plate (3) Light microscopy.

FIG. 1. Camera Lucida drawing of the fluke showing the oral sucker S, oesophagal gland G, intestinal caeca I, ventral sucker X, testes T, ovary O, cirrus sac C, and excretory opening Ex. FIG. 2. Light microscope image of the fluke. tory pore opens on a slightly invaginated posterior these papillae arrangement. The tegument covering tegumental notch on the mid posterior extremity of of exvaginated cirrus has roughed surface (Plate 4. the body (Plate 4 Fig. 3). Fig. 5). At high magnification, this tegument of the Scanning electron microscopy of H. egyptia sp. cirrus appears covered with several outgrowths, n. revealed that the body surface of the fluke is some of which are bidigitate (Plate 4 Fig. 6). covered with aspinose thick tegument with deep The genital pore is situated on the mid ventral folds and ridges. Several papillae were recognized surface of the fluke just anterior to the ventral suck- around the mouth opening and the genital atrium er (Plate 5 Fig. 4). No papillae are observed on the (Plate 4 Fig .3). There are several aciliated dome- outer rim of the ventral sucker (Plate 4 Fig. 7). shaped papillae on the surface of the fore body, which are more numerous in the region between The present trematode was found to be hitherto the oral and ventral suckers. Some of these papil- undescribed and given the name H. egyptiaÆ lae possess central openings with cilia protruding from them (Plate 4 Fig. 4). Discussion The oral sucker is surrounded by large number The investigation of the present Hamacreadium of smooth papillae, which lack any opening or species showed a close resemblance with H. dia- pores (Plate 4 Fig. 4). There is no distinct pattern of copae Nagaty et al. (1962) that was described from Pseudoplagioporus interruptos Durio... 183

Plate (4) Scanning electron micrographs.

FIG. 3. Whole body of the fluke showing oral suckers S, genital atrium G, ventral sucker X Æ Fig. 4. High magnification of the anterior end of the fluke showing the oral sucker S, genital atrium G, tegumental papillae (arrows). FIG. 5. High magnification of the genital atrium showing the protruded cirrus. FIG. 6. High magnification of the tegumental surface of the cirrus. FIG. 7. The tegument around the ventral sucker XÆ

Diacope fulviflama in the Red Sea. The two spe- it differs in having an unlobulated ovary situated cies are closely similar in many respects including close to the ventral sucker. Table 3 shows a com- the shape of the body, the situation of each of the parison between the present species of Hamacrea- ventral sucker, cirrus sac and testes. However, the dium and the other close species. present species differs from the above mentioned species in having vitelline glands extending from The present species differs from H. diacopae oral sucker to the posterior end of the body. Also, Nagaty and Abdel Aal (1962) in the size of the 184 N.E. Abdou et al.

TABLE 3. A comparison between the present description of Hamacreadium egyptia sp. n. and the related species.

H. diacopae (Nagaty H. khalili (Ramadan, H. mutabile (Linton, Present description Characters et al., 1962) (1983) 1910) H. egyptia sp. n. Body: length (mm) 1.7 - 3.1 2.9 - 6.5 2.2 1.2 Body: width (mm) 0.83 - 1.1 2.5 - 3.3 0.92 0.52 Oral sucker: length (mm) 0.21 - 0.32 0.20 - 0.40 0.23 0.13 Oral sucker: width (mm) 0.23 - 0.31 0.20 - 0.40 0.20 0.10

Ventral sucker: length (mm) 0.29 - 0.53 0.42 - 0.72 0.42 0.19 Ventral sucker: width (mm) 0.37 - 0.51 0.41 - 0.80 0.40 0.19 Oesophagus: length (mm) 0.05 0.14 - 0.57 0.23 0.10 Oesophagus: width (mm) – – – 0.11 Testes Anterior: length (mm) 0.18 - 0.26 0.40 - 1.02 0.29 0.05 Anterior: width (mm) 0.11 - 0.21 0.32 - 0.62 0.20 0.06 Posterior: length (mm) 0.18 - 0.26 0.42 - 0.97 – 0.06 Posterior: width (mm) 0.10 - 0.18 0.38 - 0.71 – 0.06 Ovary: length (mm) 0.16 - 0.21 0.10 - 0.52 0.15 0.034 Ovary: width (mm) 0.09 - 0.24 0.20 - 0.74 0.17 0.027 Lobulated Lobulated Non lobulated Non lobulated Vitelline glands aggregated in two from the intestinal from oesophagus from oral sucker level distribution groups furca to the posterior level to posterior end to the posterior end of end of the body the body Hosts Lethrinus mahsena, Lutjanus Diacope fulviflama Lethrinus mahsena, L. L. nebulosus fulviflamma, L. (Hebra) nebulosus russelli Locality Hurghada, Red Sea Arabian Gulf Hurghada, Red Sea Hurghada, Red Sea body and the internal organs (Table 3). In addition Cribb (1989) in the body shape; distribution of the to the fact that the vitelline glands never extend far vitellaria; and in size and position of the ventral anteriorly to the area of the oral sucker in H. dia- sucker (Table 3). copaeÆ Because of the lack of SEM studies on members The present material could also be differentiated of the family Opecoelidae making a comparison of from H. khalili Ramadan (1983) infecting the Red the present materials with other species is difficult. Sea fish Lethrinus mahsena and L. nebulosus in the The aspinous tegument was recorded from Gor- shape and size of the body, in possessing a large goderina attenuata (Nadakavukaren and Nollen, ventral sucker situated at the middle of the body 1975); Leucochloridium sp. (Bakke, 1976); Con- (Table 3) and the distribution of the vitellaria. cinnum epomopis (Otubanjo, 1985) and Phyllodis- It also differs from the description of H. muta- tomum umblae (Bakke and Baily, 1987). bile Linton, 1910 given by Saoud et al. (1987) The fluke surface of the present material is en- from Lutjanus fulviflamina and L. russelli from the circled by tegumental folds or ridges at irregular in- Arabian Gulf in the distribution of the vitellaria, tervals. Those ridges have big protuberances or which extend from the intestinal furca to the poste- Cobblestone-like cytoplasmic process that give a rior end of the body and in the shape and position spongy appearance to the tegumental surface. A of the ovary. similar pattern of ridges was observed on the tegu- Hamacreadium egyptia n. sp. differs from H. ment of the most of the previously mentioned trem- mutabile Linten, 1910 described from Lutjanus atodes, for example Gorgoderina attenuata (Nada- amabilis from Queensland-Australia by Bray and kavukaren and Nollen, 1975); Leucochloridium sp. Pseudoplagioporus interruptos Durio... 185

(Bakke, 1976); Metagonimus yokogawai (Lee et Few studies have been done on the fine structure al. 1984); Concinnum epomopis (Otubonjo, 1985) of these papillae. Recently, in 1993 _drsk made a and Phyllodistomum umblae (Bakke and Bailey, transmission electron microscope study on the ven- 1986). tral sucker papillae of Brachylaimus aequans and divided these papillae into three types according to Nadakavukaren and Nollen (1975) assumed that the internal receptor structure. His study revealed the ridges on the tegument are caused by contrac- the presence of nerve fibre running from the recep- tion waves of the internal musculature of the fluke. tors to the nerve trunk as described early in juve- Also, he suggested that the tegumental protuber- nile trematode, Gorgoderina vitelliloba by Hoole ances may serve to increase the surface area for ab- and Mitchell (1981). According to these results it sorptive functions of tegument much like the mi- could be proposed that these papillae are function- crotriches of cestodes. Otubanjo (1985) agreed ing as sense organs to the fluke. with Nadakavukaren that the formation of large body folds and ridges increase the surface area of Bakke (1976) mentioned that the domed papillae trematode. seem to be a fundamental type that have been fre- quently recorded in trematodes, and he believed Two types of sensory papillae on the fore body that they have a sensory function. Frederichsen surface, ciliate-dome shaped papillae and aciliate- (1978) also assumed that the dome shaped papillae dome shaped papillae, are present. The first type of appear to be an opening of goblet-like gland cells, papillae was previously described from Fibricola while the unciliated papillae appear to be sensory. seoulensis (Seo et al., 1984 & 1985); Hetero- Details of the terminal genitalia were used in the phyopsis continua (Hong et al., 1991). The SEM classification of digenetic trematodes by Yamaguti investigation on the surface of Leucochloridium (1971); Bakke (1976). sp. (Bakke, 1976) and Phyllodistomum conosto- mum revealed the presence of domed aciliate pa- In the present investigation the cirrus surface pillae on the surface of the fluke. was found covered by papillae in a specific pattern. This pattern shows similarity with description of The distribution pattern of papillae on the trema- the cirrus morphology of two echinostomes trema- tode surface was found to be different among dif- tode, Echinostoma revolutum and Isthmiophora ferent families. For example: It may have a regular melis, given by Smales and Blankespoor (1984). In pattern of distribution arranged in circles; lines; or E. revolutum, the cirrus tegument is smooth and in symmetrical groups such as those reported in has fine ridges. In Isthmiophora melis, the cirrus Phyllodistomum conostomum; Fibricola seoulensis has the tegumental pattern similar to that of the (Seo et al., 1984); Phyllodistomum umblae (Bakke body surface with papillae scattered over the visi- and Bailey, 1987); Echinostoma cinetorchis (Lee ble portion. et al., 1992); and Heterophyes nocens (Chai et al., As regards the geographical distribution of genus 1992). However, in some other cases, the papillae Hamacreadium, many species of this genus were distribution is random such as in Gorgoderina atte- described from different hosts in different loca- nuata (Nadakavukaren and Nollen, 1975); and tions. Leucochloridium sp. (Bakke, 1976). – In Egypt: Hamacreadium mutbile was rede- The functions of several types of papillae re- scribed from Serranus merra, L. mahsena, L. nebu- main speculative for all helminths. Edwards et al. losus, Teuthis marmorata and Diacope fulviflamma (1977), Hoole & Mitchell (1981) and Smales & in the Red Sea by Nagaty (1941). Hamacreadium Blankespoor (1984) suggested that these papillae mutabile Linton, 1910 from Lethrinus mahsena, L. are mechano and chemo-receptors that serve as- nebulosus, Epinephelus chlarostigma, E. summa- sessment of the host environment (Ciliated papil- na, and Anampses caeruleopunctatus, H. grarda- lae are usually ascribed tango-, rheo-, and chemo- gense from Variola louti; and H. khalili from Leth- receptive function, whereas, dome-shaped papillae rinus mahsena and L. nebulosus were redescribed have been shown to have a secretory function). from the Red Sea by Ramadan (1983). 186 N.E. Abdou et al.

Hamacredium caranxi (Saoud et al. 1977) was and covering the entire body. The body tegument is described for the first time from a Paciform fish, aspinous and characterized by the presence of sev- Caranx altissimus in the coastal water of Suakin, eral folds. Two types of sensory papillae, ciliate- Sudan (an old deserted part on the Red Sea). The dome type and aciliate-dome type are scattered on same authors, Saoud et al. (1986 and 1987) rede- the body tegument in irregular pattern. The cirrus scribed Hamacreadium mutabile Linton (1910) tegument is spongy and free from papillae howev- from Lethrinus nebulosus; Epinephelus tauvina; E. er, two groups of ciliated papillae are present chlorostigma; E. areolatus and E. summana from around it fishes of Arabian GulfÆ Hosts : Lethrinus nebulous and L. mehsena In Japan, Yamaguti (1934) described H. epi- Location : Intestine nepheli from Epinephelus akaara and Lethrinus Locality : Hurghada-Red Sea, Egypt. haematopterus. Moreover, H. mutbile was also re- corded from Lethrinus sp. in Fiji by Manter (1963). Type specimens: Deposited at the University of The same species was redescribed from Lutjanus Nebraska State Museum, Systematic research col- sp., L. amabilis, L. fulviflamma and Lethrinus va- lection numbers HWML 39567 (one slide). Senior riegatus from New Caledondia by Manter (1968). author has additional samples in her collections.

Hamacreadium interruptus Nagaty (1941) was References redescribed by Fischthal and Kuntz (1965) from Bakke, A. (1976) Functional morphology and surface topogra- from North Borneo-MalaysiaÆ phy of Leucochloridium sp. (Digenea) revealed by scan- Hamacreadium mutabile from Lutianus rivula- ning electron microscope, Z. Parasitenk, 51: 115-128. –––––––––– and Bailey, R.E. (1987) Phyllodistomum umblae tus, and L. fulviflamma was redescribed by Hafee- (Fabricius) (Digenea, Gorgoderidae) from British Co- zullah (1971). He also described two new species, lumbia samonids: A description based on light and H. krusadaiensis from L. frenatus and H. leiogna- scanning electron microscopy, Can. J. Zool. 65: 1703- thi from Leiognathus daura from Bengal and Ara- 1712. bian Sea, India. Bilqees, F.M. (1980) A record of five trematodes from the fishes of Karachi coast, Pakistan. Acta Parasit. Polon., Pritchard (1966) redescribed H. mehsena Na- 15: 107-114. gaty (1941) from the Hawaiian fishes. This species Bray, R. A. and Cribb, T.H. (1989) Digeneans of the family was originally described from the Red Sea. Opecoelidae Ozaki, 1925 from the southern Great Barri- er Reef, including a new genus and three new species, J. Summary Nat. Hist., 23: 429-473. Chai, J.Y., Chung, H.L. and Choi, M.H. (1992) Surface ul- Pseudoplagioporus interruptus Durio & Manter trastructure of Heterophyes nocens (Trematoda: Hetero- (1968) is a pinkish Opecoeliid trematode obtained phylidae), Korean. J. Parasit., 30: 75-82. from the intestines of Lethrinus nebulous and L. Durio, W.O. and Manter, H.W. (1968) Some digenetic trem- mehsena fishes. It is distinguished by the interrup- atodes of marine fishes of New Caledonia. Part II. Ope- coelidae and Lepocreadiidae, J. Parasitol., 54: 747- tion of the vitelline glands in two lateral groups, 756. ovary is submedian between the two testes. The Edwaras, H.H., Nollen, P.M. and Nadakavukaren, M.J. body tegument is smooth and has several pores (1977) Scanning and transmission electron microscopy however, it has a lobulated papillae in the distance of oral sucker papillae of Philophthalamus megalurus, between the oral and ventral suckers. Cobblestone- Int. J. Parasitol., 7: 429-437. like processes are elevated from the tegument of Fischthal, J.H. and Kuntz. (1965) Digenetic trematodes of fishes from North Borneo (Malaysia), Ibidem., 32: 63- the ventral sucker. 71. Hamacreadium egyptia sp. n. is a small whitish ––––––––––, Melles, J. and Buttner, D.W. (1984) Electron Opecoeliid trematode infecting the intestine of microscope study of the body wall and the gut of adult Loa loa, Z. Parasitenkd, 70: 525-536. Lethrinus nebulous and L. mehsena fishes It has a Æ Fredericksen, D.W. (1978) The fine structure and phyloge- relatively big ventral sucker in the middle of the netic position of the Cotylocidium larva of Cotylogaster body. The intestinal caeca are unequal, and the cir- occidentalis Nickerson, 1902 (Trematoda: Aspidogastri- rus is well developed. Vitelline glands are small dae), J. Parasitol., 6: 961-976Æ Pseudoplagioporus interruptos Durio... 187

Grabda-Kazubska, B. (1980) Euryhelmis zelleri sp. n. and coeliid trematode, Concinnum epomopis Sandground Euryhelmis squamula (rudolphi, 1819) (Trematoda, 1973, Z. Parasitenkd., 71: 495-504. Heterophyidae), metacercariae from Rana temporaria Pritchard, M.H. (1966) Studies on digenetic trematodes of L., from the Babia Gora National Park, Poland, Acta Hawaiian fishes, Family: Opecoelidae, Zoologi. Jahrb. Parasitol. Polonica, 15: 115-128. (Systematik), 93: 173-202. Hafeezullah, M. (1971) Opecoelid trematodes of marine fish- Ramadan, M.M. (1979) Studies on Helminth Parasites of es of India, Parasitology, 62: 321-329. Some Red Sea Fishes, Ph.D. Dissertation, Faculty of Hong, S.J. Chai, J.Y. and Lee, S.H. (1991) Surface ultra- Science, Ain Shams University, Egypt. structure of the developmental stages of Heterophyopsis –––––––––– (1983) A review of the trematode genus Hama- continua (Trematoda: Heterophyidae), J. Parasitol., 77: creadium Linton 1910 (Opecoelidae), with descriptions 613-620. of two new species from the Red Sea fishes, Jap. J. Par- Hoole, D. and Mitchell, J.B. (1981) Ultrastructural observa- asit., 32: 531-539Æ tions on the sensory papillae of juvenile and adult Gor- Saoud, M.F.A., Abu Sinna, H. and Ramadan, M.M. (1977) goderina vitelliloba (Trematoda: Gorgoderidae), Int. J. On Hamacreadium caranxi n. sp. (Trematoda: Allo- Parasitol., 11: 411-417. creadidae); An intestinal parasite of a perciform fish Lee, S.H., Seo. B.S., Chai. J.Y. and Hong S.J. (1984) Study from the Red Sea, J. Egypt. Soc. Parasit., 7: 181-188. on Metagonimum yokogawai (Katsurada, 1912) in Ko- –––––––––– and Kawari, K.S.R. (1986) Helminth parasites rea. VII Electron microscopic observation on the tegu- of fishes from the Arabian Gulf. 1. Preliminary general mental structure. Korean. J. Parasit., 22: 1-10. survey of fishes mainly from Qatari waters, Qatar Univ. ––––––––––, Son, W.M. and Hong S.T. (1987) Scanning Sci. Bull., 6: 199-229. electron microscopical findings of Echinochasmus ja- –––––––––– (1987) Helminth parasites of fishes from the Ara- ponicus tegument, Korean J. Parasit., 25: 51-58. bian Gulf. 2. The digenetic trematode genera Hama- ––––––––––, Jun, H.S., Son, W.M. and Chai, J.Y. (1992) creadium Linton, 1910 and Cainocreadium Nicoll, Tegument ultrastructure of juvenile and adult Echinos- 1909, Qatar Univ. Sci. Bull., 232-245. toma cinetorchis, Korean. J. Parasit., 30: 65-74. Seo, B.S., Lee, S.H., Chai, J.Y. and Hong, S.T. (1984) Stud- Manter, H.W. (1963) Studies an digenetic trematodes of ies on intestinal trematodes in Korea. X. scanning elec- Fishes of Fiji. II. Families Lepoereadiidae, Opisthole- tron microscopic observation on the tegument of Fibri- betidae, and Opecoelidae, J. Parasitol., 49: 99-113. cola seoulensis, Korean. J. Parasit., 22: 21-29. Miller, F.H. Tulloch, G.S. and Kuntz, R.E. (1972) Scanning –––––––––– Cha, I.J., –––––––––– (1985) Studies on intesti- electron microscopy of integumental surface of Schis- tosoma mansoni, J. Parasitol., 58: 693-698. nal trematodes in Korea. XIX. Light and scanning elec- Murakami, M. (1977) Modified TAO. Murakami Procedure, tron microscopy of Fibricola seoulensis collected from Arch. Histo., 40: 119. albino rats treated with Praziquantel, Korean J. Parasit., Nadakavukaren, M.J. and Nollen, P.M. (1975) A scanning 23: 47-57. electron microscopic investigation of the outer surfaces Smales, L.R. and Blankespoor, H.D. (1984) Echinostoma of Gorgoderina attenuata, Int. J. Parasitol., 5: 591- revolutum (Froelich, 1802) Looss (1899) and Isthmio- 595. phora melis (Schrank, 1788) Luhe, 1909 (Echinostomat- Nagaty, H.F. (1941) Trematodes of fishes from the Red Sea. inae, Digenea): Scanning electron microscopy of the II. The genus Hamacreadium Linton, 1910 (Family Al- tegumental surfaces, J. Helminthol., 58: 187-195. locreadiidae) with a description of two new species, J. Yamaguti, S. (1934) Studies on the helminth fauna of Japan. Egypt. Med. As., 24: 300:310. Part I. Trematodes of fishes, Jap. J. Zool., 5: 249-541. –––––––––– and Abdel El Aal, T.M. (1962) Trematodes of –––––––––– (1938) Studies on the Helminth Fauna of Japan, fishes from the Red Sea. Part 15. Four new species of Part 21, Trematodes of fishes IV (Kyoto: S. Yamaguti), Hamacreadium (Family Allocreadiidae), J. Parasitol., 139 p. 48: 384- 386. –––––––––– (1942) Studies on the Helminth Fauna of Japan. –––––––––– (1969) Trematodes of fishes from the Red Sea. Part 39. Trematodes of fishes Mainly from Naha, Bioge- Part. 18. On two new and one known allocreadiid spe- og. Tokyo, 3: 329-397. cies, J. Egypt. Ver. Med. Associat., 29: 1-5. –––––––––– (1971) Synopsis of Digenetic Trematodes of Ver- Otubanjo, O.A. (1985) Scanning electron microscopic stud- tebrates, Keigaku Publishing Co. Tokyo, Vol. 1, 1074 ies of the body surface and external genitalia of a dicro- p., Vol. 2, 349. 188 N.E. Abdou et al.

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