Asian Pacific Journal of Tropical Biomedicine (2012)S1064-S1069 S1064

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Document heading doi:10.1016/S2221-1691(12)60362-1 襃 2012 by the Asian Pacific Journal of Tropical Biomedicine. All rights reserved. Three new species of cercariae from praemorsa (L. 1758, Buccinum) snails in Al-Bathan fresh water body, Palestine Sami Bdir, Ghaleb Adwan* Department of Biology and Biotechnology, An-Najah N. University, P. O. Box (7)-Nablus, Palestine

ARTICLE INFO ABSTRACT

Article history: Objective: Melanopsis praemorsa To investigate other new species of cercariae encountered in 30 2012 M. praemorsa Methods: M. praemorsa Received June ( ) snails collected from Palestine. A total of 1 100 were 5 2012 Received in revised from July collected from Al-Bathan water body, Palestine, from November, 2010 to November, 2011. A 7 A 2012 M. praemorsa Results: ccepted ugust Cercariae in were obtained by emerging and crushing methods. Other Available online 28 August 2012 three new different specCercariaies of ce melanopsircariae ha vpalestiniae been identified from this sCercarianail. The smelanopsie species ( ) ( palestiniawere Xiphidiocercaria Cercaria melanopsi IV , palestiniaMicrocercous Keywords: ) ( ) M. praemorsa V and Longifurcate cercaria VI . The infection rate of Melanopsis praemorsa with these three different cercariae was (42.2%). Coinfection with Xiphidiocercariae Digenetic Trematodes and Longifurcate cercariae or Xiphidiocercariae and Microcercous cercariae has been noted and 1 23 Cercariae coinfection rate was . % among the infected snails. The highest cercarial infection rate was in (64 3 ) Longifurcate cercaria June . % . No infected snails were found in September. It was also noted that infected snails 17 22 Xiphidiocercaria attained a larger sConclusions:ize than unin fected ones and all infected snails had a size between - mm ( 20 ) Microcercous cercaria average mm . Our studies imply that there are potentially more nM.ew praemorsaspecies of Palestine trematodes in this area than were found until now. Due to the presence of infected and may be species of other snails, water resources could be contaminated by the emerging new cercariae, consequently attack the local people directly via the skin or are transferred to them by metacercariae ingestion. More surveys are needed to identify the real prevalence of the trematodes both in human and hosts, and also to determine the range of snail hosts of the parasite in enzootic areas of the disease, as well as the life cycle and biology of trematodes and its effects on man should be elucidated.

1. Introduction it is considered one of the most abundant snails present in fresh water bodies especially in Al-Bathan freshwater Freshwater snails play a vital role in the life cycle of body[3]. digenetic trematodes. These snails provide these parasites Three larval stages of digenetic trematodes were reported M. praemorsa with resources for development, reproduction and also from freshwater in Palestine. These larvae Cercaria melanopsi palestinia constitute a means of transport by which trematodes can were Xiphidiocercaria ( I), Cercaria melanopsi palestinia reach their next host. Most authors agree that trematodes Brevifurcate lophocercous ( Cercaria melanopsi palestinia were associated with molluscs before they adapted to other II) and Microcercous ( III) M. praemorsa hosts[1]. Trematodes are a diverse group of endoparasite [3]. Description new types of Cercariae from requiring intermediate host (molluscan and vertebrate) and and other snails from other countries has been reported in M. praemorsa definitive host to complete their life cycle. The distribution the literature. Therefore, it is expected that of fresh water mollusks varies with biological, physical may act as an intermediate host for many digenetic Melanopsis praemorsa and chemical characteristics[2]. trematodes of various vertebrates in Palestine. Seven types M. praemorsa M. praemorsa ( ) (L. 1758, Buccinum) is widely prevalent in of cercariae have been found in collected freshwater bodies of the Mediterranean region. In Palestine, from Yrmouk River, Jordan[4]. These included three types of Xiphidiocercariae, one type of a Brevifurcate *Corresponding author: Ghaleb Adwan, Department of Biology and Biotechnology, lophocercous cercaria, one type of a Microcercous Cercaria, An-Najah N. University, P. O. Box (7)-Nablus, Palestine. Fax: +970-9-2383589 and two types of Pleurolophocereous Cercariae. A total E-mail: [email protected] of four cercarial families and one cercarial group were Sami Bdir et al ./Asian Pacific Journal of Tropical Biomedicine (2012)S1064-S1069 S1065 Melanopsis identified from spp as follows: Heterophyidae: Cercariae were obtained from snails by emerging or crushing Haplorchis pumilio, H. taithui, Stellantchasmus falcatus and methods. In the emerging method snails were placed in Centrocestus formosanus Echinostomatidae: Echinochasmus ; the dishes containing distilled water and then, they were milvi; Cyathocotylidae, Philophthalmidae Monostome and exposed to artificial illumination for 12 h in the lab. In the group cercariae (probably Notocotylidae)[5]. Recently, a crushing method, snails were broken with tweezers and the total of eight different cercarial types have been reported soft tissues were placed between 2 slides and squashed. M. praemorsa in from the Kura River in Recovered larval trematodes were studied alive, unstained Azerbaijan[6-9]. These cercraiae included: three types of or vitally stained (0.5% brilliant cresyl blue or 0.5% neutral stylet cercaria, four types of virgulate cercaria and one type red) specimens. Some specimens were fixed in acetic acid- of lecithodendroid cercaria. Eleven types of cercariae were formalin-alcohol (AFA) solution and subsequently stained in Melanoides detected from the freshwater prosobranch snail acetocarmine. Measurements were taken on a minimum of 10 tuberculata collected from the Nile and irrigation system specimens of live and fixed larval trematodes. The behavior in several localities of Egypt[10]. These cercariae belong to of cercariae was observed using a dissecting microscope. four main type groups: two types xiphidiocercariae, two types furcocercous cercariae, four types pleurolophocercous 3. Results and three types gymnocephalous cercariae. In addition to these, twenty four trematode species comprising 19 M. praemorsa species of cercariae and 11 species of metacercariae (six From the total of 1 100 , 464 (42.2%) snails species occurred both as cercariae and metacercariae) were infected with three different cercariae. These new Cercaria melanopsi were identified in Central Europe from Lymnaea stagnalis cercariae were Xiphidiocercaria ( palestinia Cercaria melanopsi snails[11]. IV), Microcercous cercaria ( palestinia Cercaria melanopsi In Palestine, our knowledge on freshwater larval trematodes V) and Longifurcate cercaria ( palestinia is still poor. The present study describes three new species VI). The infection rates were 31.4%, 7.0%, and M. praemorsa of cercariae encountered in specimens of 3.8% for Xiphidiocercaria, Microcercous cercaria and collected from Al-Bathan freshwater body, Palestine. Longifurcate cercaria, respectively. These cercariae have not been described before from this snail. Coinfected snails with Xiphidiocercariae and Longifurcate crcariae or 2. Material and methods Xiphidiocercariae and Microcercous cercariae has been noted but rare, and the coinfection rate was 1.23% among the M. praemorsa A total of 1 110 snails were collected from infected snails. The highest cercarial infection rate was in Al-Bathan freshwater body in Palestine from November, June (64.3%). No infected snails were found in September. It 2010 to November, 2011. Examination of snails were carried was also noted that infected snails attained a larger size than out as described previously[3]. The collected snails were uninfected ones and all infected snails had a size between kept in a glass aquarium containing water and thin layer 17-22 mm (average 20 mm). Details of measurements of the of sediment from the same habitat of snails. Aquaria various structures of each type of cercariae are presented in were continuously aerated using air pumps. Snails were Table 1. examined for larval trematodes within 2-3 d after collection. Table 1. Cercaria melanopsi palestinia IV,V VI M. praemorsa Measurements (毺m) of the various structures of and encountered in snails collected from Al- Bathan freshwater body, Palestine. Cercaria melanopsi palestinia Type of Structure IV VI VI a Body length 65-120 270-330 400-420 60-110 380-410 a Body width 40-60 70-130 210-220

35-50 200-210b a Tail length 47-75 70-90 440-460 40-70 420-440 a Tail width 8-14 50-70 100-110 Oral sucker (diam.) 25-30 55暳58 80-90暳82-93 Ventral sucker (diam.) 20-25 50暳53 28暳28 Pharynx 6暳12 23暳30 8-12 Excretery vesicle (diam) 16暳22 (50-70) 暳(40暳56) 30暳60 Flame cell formula 2[(3) + (5) + (2) + (3)]=26 [(2+2+2)+(2)]=16 2[(1+1+1+1+1+1+1)+ (1+1+1+1+1+1+1) +[(1+1+1+1)]]=36 a b Measurements are given for live (upper values) and fixed (lower values) specimens. This measurement includes the length of tail rami which are 213-222 by 44-46 毺m (live) and 200-205 by 40-44 毺m (fixed). Sami Bdir et al ./Asian Pacific Journal of Tropical Biomedicine (2012)S1064-S1069 S1066 3.1. Cercaria melanopsi Palestinia IV (Figure 1 A, B; Table a flame cell formula 2[(3+5+2+3)]=26, but are missed in the 1) tail. The anlagen of reproductive organs are found posterior and around the ventral sucker. This cercaria has a small, oval shaped and transparent These cercariae actively swim using their tail near the body with fine spined, 1-2 毺m thick tegument. The water surface, while in the bottom start wiggling rather than C. melanopsi ventral sucker which is located in posterior half of the creeping. palestinia IV develops within ovoid body, is smaller than oral sucker. This type of cercaria sporocysts measuring 87-180 毺m long by 84-160 毺m wide. I 1 2 毺 has an oral sucker, of which possesses“ not only the s”tylet t is covered with a - m thick tegument and filled with but also a peculiar structure, called virgula organ . In 1-4 fully developed cercariae, 1-2 developing cercariae, and Cercaria melanopsi Palestinia IV, the dagger-shaped several germ cells. stylet measuring 14 毺m 暳 3 毺m and a bilobed virgula that 3.2. Cercaria melanopsi Palestinia V (Figure 1 C; Table 1) covers more than the half of the oral sucker area, which contains non-granulated material. In addition, it has two pairs of penetration gland cells containing coarse granular The body of this cercaia is covered with a smooth 3 毺m matter, located antero-laterally to the ventral sucker, open thick tegument and longer than tail stem. However, several on both sides of the stylet. The digestive system consists rows of fine spines are found at the inner edges of both oral only of a mouth and a pharynx, but oesophagus and caeca and ventral suckers. The body of this cercaria is filled with are apparently absent. The excretory system consists of a refractile granules which appear to be cystogenous material. shaped like kidney excretory vesicle measuring 20-24 毺m The tail is short, stumpy, muscular, and sometime may be 暳 15-17 毺m, located at the posterior end of the body. There used for attachment. Both suckers are round, ventral sucker are two main excretory ducts, one on each side of the body. is a little bit smaller than oral sucker and located centrally These ducts extend posteriorly, to join antero-laterally the near the middle region of the body. The stylet is in the excretory vesicle. The excretory vesicle is opening into anterior edge of the oral sucker measuring 12 by 5 毺m. posterior body extremity through a caudal canal extending The digestive system consists of a mouth that leads into a posteriorly through the length of the tail to open at its tip. thin pre-pharynx which connects with an oval pharynx, Flame cells are arranged symmetrically in the body and has while oesophagous is rudimentary. This type of cercaria has

Figure 1. Cercaria melanopsi palestinia IV V M. praemorsa C. melanopsi palestinia IV , and encountered in snails from Al-Bathan. and its C. melanopsi palestinia V sporocyst (A and B), (C) and its sporocyst is not shown.

B A

Figure 2. Cercaria melanopsi palestinia M. praemorsa VI and its sporocyst (A and B) encountered in snails from Al-Bathan. Sami Bdir et al ./Asian Pacific Journal of Tropical Biomedicine (2012)S1064-S1069 S1067 three pairs of penetration glands located above the ventral ventral sucker. A total of 36 flame cells have been detected sucker. Gland ducts, on each side, form two bundles. The in Cercaria melanopsi Palestinia V, seven on each of outer outer bundle consists of two ducts, while the inner consists and inner duct, and 4 pairs along the caudal duct, flame of one duct. All bundle run anteriorly to open on both sides cells are missed in rami. of the stylet. The excretory vesicle is relatively large, filling The possible flame cell formula is 2[(1+1+1+1+1+1+1)+(1+1+1+ major portion of the space between the ventral sucker and 1+1+1+1)+[(1+1+1+1)]]=36. The genital primordium consists of the posterior end of the body. It measures 70-85 毺m by 40- relatively large cells found immediately above the excretory 56 毺m and is characterized by having a 11-14 毺m thick vesicle. The glandular system composed of 5 pairs of wall. Two main lateral ducts run anteriorly, while others 2 granular cells arranged symmetrically inside the penetration short ducts run to posterior end of the body. Flame cells are organ, and open at the anterior margin, as well as, 10 pairs of arranged symmetrically in the body but are absent in the granular cells are found outside the penetration organ. tail. Flame cells formula is 2[(2+2+2) +(2)]=16. This cercaria is a rapid swimmer but its movements are This type of cercariae shows no swimming activity, because interrupted by frequent resting pauses. As typical for it has short tail, which may developed as a sucker for furcocercous cercaria, the swimming is tail directed, and attachement. It was clear that it used the tail to attach itself when inactive, the larva sinks slowly to the bottom. This to the bottom of the water container. When detached from cercaria develops within unbranched thread-like spotrocysts the bottom the cercaria creeps, for a short period of time, located in the heptopancreas of the snails. The sporocysts in a worm- like manner using both sucker for positioning. are extremely elongated (2 700-6 300 毺m 暳 240-380 毺m), The cercaria casts off its tail and dies without encystment annulated and have one pointed end to form a birth pore. after several hour of emergence from the snail. The cercaria Sporocysts usually contain 8-14 developed cercariae, 4-12 develops in a sausage- shaped sporocysts varying greatly in developing cercariae, and germ balls. size (800-2 300 毺m 暳 380-610 毺m). The sporpcyst has a birth pore at its anterior end and is filled with many developed 4. Discussion cercariae, developing cercariae, and germ balls. 3.3. Cercaria melanopsi Palestinia VI (Figure 2 A, B ; Table This study adds more information to the trematode fauna 1) in Palestine and represents the first step to understand the host-parasite relationship including the completion of This cercaria comprises an oval body, longifurcate, non- their life cycles as well as defining their final hosts. High oculate, pharyngeate. The length of the tail stem (226-237 prevalence of infection in June, this might be due to low 毺m) is approximately the same as well as the length levels of water, slow-flowing in the stream during hot non- furcal ramus (213-222 毺m), no furcal finfolds. It is covered rainy season, also it could be due to high contamination by with 2-4 毺m thick tegument which is provided with fine the faecal matter of livestock, birds and other . It spines usually more concentrated at the anterior part of is probably that snail abundance is low in the summer and the body. A total of 7 pairs of sensory cilia found along miracidia enter most available snails. It is noted that more the tail stem measuring 14 毺m long, another four pairs of than 93% of infected snails were could not creep to the wall sensory cilia of 4 毺m long are found at each tail ramus. It of aquarium, this may be due to pathological effect of these has a rudimentary ventral sucker measuring 28 毺m 暳 28 毺 cercariae on the host. M. praemorsa m, located post-equatorial. Cercaria melanopsi Palestinia snail is apparently intermediate host for V has an oral sucker which is modified to relatively large many digenetic trematodes of various vertebrates living penetration organ measuring 80-90 毺m 暳 82-93 毺m. The in this area. Three types of cercariae have been described digestive system consists of a mouth that leading posteriorly previously and were encountered in this snail in Al-Bathan into a very short distinct pre-pharynx (6-7 毺m), followed water body[3]. Our studies revealed that this snail could by a muscular spherical pharynx (8-12 毺m), then a short carry at least six different types of cercariae in Palestine. oesophagus, as long as pharynx approximately (14 毺m), the Xiphidiocercaria was coined for the group of non-oculate oesophagus then leading into two long intestinal caeca (17-20 distome cercariae in which the tail is slender and a stylet 毺m wide) that extend to posterior extremity of the body is present at the round anterior end[12]. Development terminating close to anlagen of reproductive organs. The of these cecariae occurs in sporocysts and encystment excretory system consists of spherical excretory vesicle with takes place in intermediate hosts. The main features used a diameter (30-60 毺m). From the excretory vesicle a caudal to distinguish between Xiphidiocercariae are the size excretory duct extends posteriorly along the tail stem that of the suckers, position of ventral sucker, nature of the terminates in an opening on the tip of each caudal ramus. gut, number and position of the penetration glands, and T wo pairs of main primary excretory ducts run anteriorly, presence or absence of a fin-fold along the marg“ins of th”e the outer pair runs to about the level of penetration glands, tail. The presence of well developed stylet and virgula C. melanopsi while the inner pair runs to about the level rudimentary organ in palestinia IV identifies this type as Sami Bdir et al ./Asian Pacific Journal of Tropical Biomedicine (2012)S1064-S1069 S1068 “ ” C. melanopsi Xiphidiocercaria and belongs to Cercaria Virgulae V which was described previously from “ ” M. praemorsa subgroup[13]. Cercaria Virgulae subgroup erected snails collected from Yarmouk River, for spinous Xiphidiocercaria in which the ventral Jordan[4], except that number of pairs of penetration sucker is smaller than the oral, tail lacks a fin-fold, glands (3 vs the 5) and ventral sucker is a little smaller C. melanopsi excretory vesicle almost V-shaped, and a highly than oral sucker. Palestinia V resembles ‘ ’ Cercaria characteristic virgula organ present, consisting of that of larva of Sphaerostoma bramae ( micrura Bithynia two pyriform sacs which are fused in the median line ) which develops in a sporocyst in tentaculata C. melanopsi and have their pointed ends directed forward and [13]. However, Palestinia V Cercaria micrura situated near the oral sucker[13]. The virgula organs differs from in which the later has are residual ducts of the mucoid body gland-cells and ventral sucker larger than oral sucker; its gut consists remain after the gland cell bodies degenerate. The of a pre-pharynx, oesophagus and caeca relatively ducts are markedly enlarged and appear as paired long; has four penetration glands and the intermediate B. tentaculata C. melanopsi comma-shaped reservoir, open to the exterior and, host is . palestinia III M. praemorsa during penetration of the second intermediate host, has been recently described from in C. melanopsi release materials that forms a pseudocyst around the Palestine[3]. Palestinia V differes from C. melanopsi cercarial body to attach it to the host as penetration palestinia III in number of penetration C. melanopsi occurs[14]. palestinia IV closely related glands and flame cells. Another related microcercous C. melanopsi III M. to described previously from cercaria, C. theodoxi II has been described from praemorsa Theodoxus jordani C. snails collected from Yarmouk River, snails in Yarmouk River[16]. melanopsi Palestinia V Cercaria theodoxi Jordan[4], except that the latter having three pairs of differs from penetration glands instead of two and having 30 flame II in many aspects such as the arrangement of C. melanopsi cells instead of 26 in Palestinia IV. On penetration glands, flame cells formula and number, C. melanopsi the other hand, palestinia IV is different the larger size of the tail, the absence of long spines at C. melanopsi C. melanopsi II[4] in may aspects from . “ ” the periphery of the anterior end and the intermediate II having larger penetration glands; the Vurgula host. C. melanopsi organ is unilobed; and the ventral sucker is located The presence of forked tail in Palestinia C. melanopsi in the middle. Also Palestinia IV is VI identifies it as a fucocercous cercariae. There are C. melanopsi different from palestinia I which was two forms of fucocercous cercariae; the brevifurcate [3] “described” previously , the later differs in being the fucocercous form, the length of each of the furcal Vurgula organ is absent and having 18 flame cells. ramus is less than the half of the length of the main C. melanopsi Palestinia IV is different from Virgulate tail stem and in the longifurcate fucocercous form, Cercaria xiphidiocercariae called sp. IX Malabar n.sp each of the fucal ramus is more than half of the length Cercaria C. melanopsi and sp. X Malabar n.sp, which are described of the main tail stem[17]. Palestinia VI Thiara tuberculata recently from snails collected from is belonged to a group longifurcate fucocercous, freshwater bodies in the Palakkad district of Kerala[15]. due to the length of each rami is more than half C. melanopsi Palestinia IV is distinct from these in size of the length of the main tail stem. The presence of body and stylet, shape of virgula organ, arrangement of a pharynx, absence of eyespots, distome, this and number of penetration glands and flame cells, cercaria belongs to pharyngeal lo“ngifurca”te distome absence of intestine and also in the intermediate host. cercaria, which belongs to the Vvivax group[13]. C. melanopsi C. Rrecently, two types Virgulate xiphidiocercariae were palestinia VI closely related to melanopsi M. praemorsa described[10], these are collected from the freshwater XV described previously from Melanoides tuberculata C. prosobranch snail from the snails collected from Jarash Falls, Jordan [18]. In melanopsi Nile and irrigation system in several localities of XV, the length of the tail of the ramus is C. melanopsi Egypt. These Virgulate xiphidiocercariae are distinct about two thirds of the tail stem, while in C. melanopsi from Palestinia IV in may aspects such palestinia VI the tail ramus has a length of about the C. melanopsi as shape of stylet, virgula, genital primordium, shape same as the tail stem. XV has 16 pairs of excretory vesicle, number of penetration glands and of flame cells in the body and 5 pairs of flame cells intermediate host. Number and flame cells formulae for in the tail stem, while 14 pairs of flame cells in body C. melanopsi these Virgulate xiphidiocercariae are not mentioned. and 4 pairs of flame cells in tail stem of C. melanopsi Microcercous cercariae is one of the lesser groups palestinia VI. XV has 11 pairs of granular of cercariae, though, in recent times, a number of glands are found outside the penetration organ, while C. melanopsi both marine and fresh-water species have been palestinia VI has 5 pairs inside and 10 described [13]. Cercaria melanopsi Palestinia V pairs of granular glands outside the penetration organ. “ ” C. melanopsi belongs to a group designated as a Microcercous . Moreover, XV has finfolds covering most C. melanopsi Cercaria melanopsi Palestinia V is closely related to of the tail rami, while this is absent in Sami Bdir et al ./Asian Pacific Journal of Tropical Biomedicine (2012)S1064-S1069 S1069

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