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The Biology of Echinoparyphium (Trematoda, Echinostomatidae)

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The Biology of Echinoparyphium (Trematoda, Echinostomatidae) DOI: 10.2478/s11686-012-0042-5 © W. Stefan´ski Institute of Parasitology, PAS Acta Parasitologica, 2012, 57(3), 199–210; ISSN 1230-2821 INVITED ARTICLE The biology of Echinoparyphium (Trematoda, Echinostomatidae) Jane E. Huffman and Bernard Fried Department of Biological Sciences, East Stroudsburg, PA 18301; Department of Biology, Lafayette College, Easton, PA. 18042 Abstract Echinoparyphium species are common, widely distributed intestinal parasites causing disease in animals worldwide. Interme- diate hosts include snails, bivalves, and fish, whereas the definitive hosts are mainly birds and mammals. This review exam- ines the significant literature on Echinoparyphium. Descriptive studies, life cycle, experimental and manipulative studies, and biochemical and molecular studies are presented. The influence of environmental factors, and toxic pollutants, are reviewed as well as studies on the pathology of Echinoparyphium. Keywords Biology, Echinoparyphium, Echinostomatidae, Trematoda Introduction small intestine of Fuligula manila (scaup). Dietz (1909) re- viewed the family Echinostomidae (Poche, 1925) and erected The genus Echinoparyphium is an important taxon in the several new genera, including Echinonaryphium. Luhe (1909) family Echinostomidae. Species in this genus are of consid- proposed E. recurvatum (von Linstow, 1873). Echinopa- erable importance in medical, veterinary, and wildlife para- ryphium is a ubiquitous parasite of freshwater snails, tadpoles, sitology. Fried (2001) provided a significant review on all birds, and some mammals. aspects of the biology of numerous species in the genus in The identification of Echinoparyphium is done on the basis his review of echinostomes other than those in the genus of morphological features of adults and cercariae, in particu- Echinostoma. Since that review, a search of the ISI Web of lar, the presence of a head collar with spines arranged in a dou- Science in June, 2012, indicated that there were three re- ble row with dorsal aboral spines larger than oral ones in views concerned with subject matter of the genus Echino- adults, the presence of numerous small corpuscles in the ex- paryphium. These reviews are as follow: Toledo et al. (2009) cretory system, and a cercariae tail without finfolds (Fried and provided an update on various aspects of the biology of im- Graczyk 2000, Kostadinova 2005). portant species of Echinoparyphium; Chai et al. (2009) dis- The systematics of Echinoparyphium spp. has been char- cussed the various species of Echinoparyphium that are acterized by a long history of inadequate descriptions, poor involved in intestinal foodborne trematodiases in Southeast specific diagnoses, extensive synonymy, and other problems Asia; and Morley (2010) considered species of Echinopary- (McCarthy 1990, Kostadinova and Gibson 2000). Features phium involved in the interactive effects of parasitic disease often used for species discrimination include morphology and and pollution in aquatic molluscs. morphometry of larvae, adults, or both; host-parasite rela- tionships; geographical distribution; and molecular analyses. However, no consensus has emerged on the most reliable char- Morphology and taxonomy acteristics for species identification. In an attempt to overcome this difficulty, species have been arranged in species groups on Echinoparyphium was first described as Distomum recurva- the basis of their life cycle and morphological traits, such as tum by von Linstow, 1873 using material collected from the the number of collar spines. The Global Species web site Corresponding author: [email protected] 200 Jane E. Huffman and Bernard Fried (globalspecies.org) lists the following species of Echino- Diaz Diaz (1976) obtained cysts from experimentally in- paryphium: E. aconiatum, E. agnatum, E. baculus, E. baqulai, fected L. peregra reared in the laboratory and fed experi- E. chinensis, E. cinctum, E. clerci, E. contiguum, E. elegans, mental bird hosts. The birds (pigeons, chicks and domestic E. flexum, E. harveyanum, E. hydromyos, E. japonicum, ducks) were each fed 25 to 30 day old metacercariae (previous E. kashmirensis, E. macrovitellatum, E. mordwilkoi, E. multi- infections with 2 to 4 day old cysts did not result in infections). ovatus, E. nordianum, E. oscitansi, E. paracinctum, E. pa- Mature E. recurvatum were found in the small intestine 10 raulum, E. petrowi, E. phalacrocoracis, E. phasianinum, days post-infection. The eggs are unembryonated when laid, E. pindchi, E. politum, E. recurvatum, E. rubrum, E. scaptero- golden yellow in color, thin-shelled and operculate. A mor- mae, E. schulzi, E. sinorchis, E. sisjakowi, E. skrjabini, E. syr- phological description of redia and cercaria was reported by dariense, E. westsibiricum. The site also provides the Faltynkova et al. (2008). definitive host for the species of Echinoparyphium. Kanev Kanev et al. (1998) reported on the characteristics of (1990) published a checklist of the genus Echinoparyphium E. rubrum based on experimental evidence of the life cycle. consisting of 151 species names. Approximately 45 names All stages of the life cycle of E. elegans were described by represented the 43 collar-spine adult worms, most of which means of light and scanning electron microscopy by King and are incompletely described and their life cycles unknown. Van As (1996). Sohn et al. (2002) observed the tegumental ul- Morphological descriptions for the life cycle stages of trastructure of E. recurvatum according to developmental E. recurvatum was provided by Diaz Diaz (1976). The cercaria stages. Worms (1, 3, 5 and 15-day old) were recovered from of E. recurvatum emerge throughout the day in a moderate chicks experimentally infected with metacercariae from Radix number, but the greatest number are shed between 9 and 12 in auricularia coreana. It was confirmed that the surface ultra- the morning. They swim actively, exhibit a creeping motion structure of E. recurvatum was generally similar to that of and remain alive for about 24 hours. The redia of E. recurva- other echinostomatid flukes. However, some features, i.e., tum are located in the digestive gland of infected snails. The morphological change of tegumental spines and appearance redia are packed with numerous elongate rediae of various of sensory papillae on the ventral sucker according to devel- sizes. The redia are very active. The body tegument is thick opment, and number, shape and arrangement of collar spines, and in mature rediae it is covered with small dark-green pig- were characteristic, which may be of taxonomic and bioeco- ment spots whereas the younger rediae are almost colorless. logical significance. Eight to nine mature cercariae are present at the same time, to- The surface topography of 15-day-old adult E. recurvatum gether with a small number of immature cercariae. As soon as sensu stricto, from an isolate of the parasite utilizing Lymnaea the cercariae emerge from the snail host, they begin swimming peregra as first intermediate host in southern England, was movements which continues until they make contact with a described and illustrated using scanning electron microscopy snail. They crawl about on the surface of the snail using the by McCarthy (2011). The results were compared to those of oral sucker and acetabulum until penetration and encystment other Echinoparyphium species from Europe, and with those take place. The snail Lymnaea peregra is utilized by the cer- of E. recurvatum of East Asian origin. The value of SEM stud- caria of E. recurvatum as both primary and secondary inter- ies may prove valuable in elucidating the relationship between mediate host. Additional laboratory-bred snails L. stagnalis, members of the genus Echinoparyphium in Britain/Europe and Physa fontinalis. Planorbis carinatus and P. corneus are also those in Africa, Asia and North America. intermediate hosts. The encysted metacercariae in both natu- rally and experimentally infected snails are located in the man- tle cavity and digestive gland but are occasionally found in the Life cycles wall of the esophagus and intestine (Diaz Diaz 1976). The cysts of E. recurvatum are almost circular in outline, The life cycle of E. recurvatum was demonstrated experi- and contains a relatively inactive metacercaria which is mentally by Mathias (1927) after feeding encysted stages of tightly coiled and occupies the whole of the lumen of the an echinostome cercaria from Planorbis planorbis to ducks. cyst. The cyst wall is transparent and consists of an outer Harper (1929) experimentally completed the life cycle of hyaline layer and thick inner layer. After 15 days the oral this species. Azim (1930) obtained the adult parasites after sucker, pharynx, and acetabulum are slightly increased in feeding dogs, white rats and wild rats with metacercariae size and although the collar spines become more conspicu- from several species of Bulinus. Sohn (1998) observed the ous they are difficult to count on the coiled body of the characteristics of the life history of E. recurvatum under metacercaria. The penetration and cystogenous gland-cells both natural and laboratory conditions. Riech (1927) have completely disappeared and the intestinal caeca has be- demonstrated the life cycle of E. aconiatum. The life cycle come indistinct. The most prominent features of the metac- of E. flexum was described by McCoy (1928) and Najarian ercariae are the main excretory ducts, their contents and the (1953, 1954) experimentally determined the life cycle of beating cilia in the secondary ducts. The size
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