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 (, )

Jane E. Huffman and Bernard Fried Department of Biological Sciences, East Stroudsburg, PA 18301; Department of Biology, Lafayette College, Easton, PA. 18042

Abstract Echinoparyphium are common, widely distributed intestinal parasites causing disease in worldwide. Interme- diate hosts include , bivalves, and , whereas the definitive hosts are mainly birds and . 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 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- . 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 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; -parasite rela- tionships; geographical distribution; and molecular analyses. However, no consensus has emerged on the most reliable char- Morphology and 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- 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-. The 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 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 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 the cercariae emerge from the 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. 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 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, , 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 . 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 of the cysts re- E. flexum. mained essentially unchanged during development (Diaz Echinoparyphium hydromyos sp. nov. with forty-five col- Diaz 1976). lar spines was described from the Australian water rat, Hy- The biology of Echinoparyphium (Trematoda) 201

Table I. Some avian hosts for Echinoparyphium

Species Number of Host Geographic Reference spines distribution E. aconiatum 45 Aves Europe/Asia/USA Alishauskaite 1960 E. agnatum Unknown Anas platyrhynchos Kashmir Ahmad and Chishti 1997 domesticus Netherlands Borgsteede et al. 2003 Birds of Prey E. clerici 41 Anas platyrhynchos Kashmir Dar and Ahmad 1992 domesticus E. dunni 43 Anseriformes/ Asia () Lie and Umathevy 1965 Columbiformes/ Passeriformes E. elegans 43 Anseriformes/ Africa Mouahid and Mone 1988 Ciconiiformes/ Strigiformes Domestic chickens/ pigeons/canaries* E. flexum 45 Gruiformes/ Anseriformes/ North America Najarian 1953 and 1954 Galliformes/ Columbiaformes E. kashmirensis Unknown Domestic Fowl* Kashmir Chishti and Tanveer 1992 E. limosorum 48-51 Limosa limosa Eastern Europe Macko et al. 2009 (Black-tailed Godwit) E. megacirrus 43 Domestic Chicken* Argentina Viozzi et al. 2005 E. montgomeriana Unknown Aves South Africa Appleton et al. 1983 E. mordwilkoi Unknown Vanellus vanellus Eurasia Grabda-Kazubska and (Northern Lapwing) Kiseliene 1991 E. oscitansi Unknown Anastomus oscitans Thailand Poonswad and Chatikavanij (Asian open billed stork) 1989 E. petrowi 49 Domestic Chicks* Russia Nevostrueva 1953 E. pindchi 35 Aquatic Migratory Birds Dar and Kharo 1991 E. pseudorecurvatum 45 Domestic Chicks* Poland Kiseliene and Grabda-Kazubska 1990 E. ralphaudyi 43 Domestic Chickens, Egypt, Ethiopia Lie et al. 1975 Ducklings* E. recurvatum 45 Anser anser North America Hosseini et al. 2001 (Gray lag goose) New Zealand Latham and Poulin 2002 Larus dominicanus Czech Republic Sitko 1998 Taft et al. 1993 (Southern black-backed gull) Macko et al. 2004 Buteo buteo hawks and owls Fredensborg et al. 2004 Charadrius hialicula Larus Pence et al. 1980 novaehollandiae scopulinus Davidson et al. 1977 (Red billed gull) Pheasant McJunkin et al. 2003 Ruffed Grouse Wild Turkey Canaris and Kinsella 2000 Shore Birds E. rubrum 43 Buteo jamaicensis North America Kanev et al. 1998 (Red tail hawk) E. serratum 37 Ducklings and chickens* Howell 1968b E. spinosus Unknown Vanellus spinosus India Singh et al. 2002 (Spur winged plover) E. speotyto 41 Speotyto cunicularia Oklahoma Buscher 1978 (Burrowing Owl) Echinoparyphium sp. Unknown Ciconia ciconia Germany Schuster et al. 2002 ()

* Laboratory infected hosts. dromys chrysogaster by Angel (1967). The cercaria occurs Echinoparyphium serratum sp. nov., with 37 collar spines, naturally in Plananisus isingi and all stages in the life-history was described from experimentally infected ducklings and have been demonstrated experimentally. Encystation occurs chickens. It appears to be most closely related to E. aconiatum in the kidneys of tadpoles. The adult is most closely related to but differs from it in having smaller eggs, fewer tegument E. recurvatum. E. recurvatum occurs predominantly in birds, spines, almost confluent vitellaria in the post-testicular region, and is rarely found naturally in mammals. E. hydromyos has and the inner margin of the ventral sucker is serrated. The nat- been found only in a . ural host is unknown but thought to be a bird. 202 Jane E. Huffman and Bernard Fried

Table II. Mammalian hosts infected with Echinoparyphium

Species Number of spines Definitive host Intermediate host Geographic location Reference E. combesi 43 Laboratory Mice* Bulinus truncates Algeria Kechimer 1980 Physa acuta Rana ridibunda perezi tadpoles E. contiguum 37 Muskrat Unknown Nebraska Barker 1915, 1916 (Ondatra zibethicus) E. elegans 43 Laboratory Rats* Caficophoron micro- South Africa King and Van As 1996 Domestic Cat* bothrium Moema, 2011 E. hydromyos 45 Water Rat (Hydromys Plananisus isingi Australia Mulder and Smales chrysogaster) 2006 Duky Rat (Rattus colletti) E. rubrum 43 Golden Hamster* Physa gyrina Michigan, Kanev et al. 1992, (Mesocricetus Physa occidentalis Wisconsin, 1998 auratus) Indiana E. recurvatum 45 House Rat Unknown Korea Lee et al. 1990 Human Egypt Fain and Galal 1977 E. sisjakowi 37 Muskrat Viviparid snails Viviparid snails Ivanov and (Ondatra zibethicus) Semenova 2000 Echinoparyphium sp. Unknown Arctic Fox Unknown Greenland Rausch et al. 1983 Alopex lagopus

*Laboratory infected host

Bile composition may account for the markedly different Kechemir (1980) described the adult and developmental recovery percentages of adult worms from the two experi- stages and life cycle of E. combesi. Sporocysts and rediae de- mental hosts. Miracidia hatch between 9 and 11 days at 22°C. velop in Bulinus truncatus. In natural conditions cercariae re- Experimental infections of snails with miracidia have not been leased by the snail Bulinus encyst in the pericardial cavity of obtained. Rediae occur naturally in Isidorella brazieri Smith, Physa acuta and B. truncatus itself. Experimentally they may and free-swimming cercariae encyst in the pericardium of the encyst in Planorbarius metidjensis and also in the kidneys of same species of snail. This latter part of the life-cycle is based Rana ridibunda perezi tadpoles. They can also encyst in situ on strong circumstantial evidence. A few cysts were occa- in the first intermediate host. Experimentally, metacercariae sionally found in the pericardium of Lenameria sp. but the en- mature in the small intestine of chicks and mice. closed metacercariae were dead. The cercaria can be Nevostrueva (1953) described E. petrowi from chicks, distinguished from Cercaria echinata, the cercaria of E. aco- ducklings and goslings infected with metacercariae obtained niatum, and C. equispinosa in having cystogenous gland cells from Viviparus viviparous. The new species has 49 cephalic containing granular material only, and the inner margin of the spines which distinguishes it from all other species of the ventral sucker is serrated (Howell 1968a). genus in which the greatest number of spines is 45. The life cycle and morphology of E. ralphaudyi sp. nov. During a survey of parasites of the Patagonian freshwater was described by Lie et al. (1975). Natural infections were crab Aegla neuquensis neuquensis, its ectosymbiont Temno- found in Bulinus truncatus from Egypt, Ethiopia, and the cephala chilensis was found parasitized with an echinostom- Yemen Arab Republic, and later in B. forskalii and B. serici- atid metacercaria with 43 collar spines. Of the 414 T. chilensis nus from Ethiopia. The sporocysts of this species develop near collected, 106 were parasitized with metacercariae of the places of miracidial entry into the snail (the head-foot re- Echinoparyphium sp. Ovigerous adults of E. megacirrus were gion, mantle edge, pseudobranch, and antennae). Rediae occur obtained from domestic chicks experimentally infected with mainly in the ovotestis and in tissues anterior to the liver. The metacercariae obtained from temnocephalans (Viozzi et al. first cercariae are released 24 days postexposure. Metacer- 2005). cariae encyst in various freshwater snails and are localized in Echinoparyphium montgomeriana, was described from the pericardial sac and the posterior part of the kidney. Adult Durban, South Africa. The adult fluke is a parasite of the ali- worms live in the small intestine of a variety of experimental mentary tract of birds. Its larval stages are common parasites of animals: hamsters, rats, mice, chicks, ducklings, pigeons, and freshwater snails belonging to the family includ- finches (Lie et al. 1975). ing Bulinus africanus. These intra-molluscan stages are shown The life cycle of E. elegans Looss, 1899 was described by to have a seasonal transmission cycle (Appleton et al. 1983). King and Van As (1996). Adults of this parasite were obtained The life cycle of E. dunni, a 43-spined species was by feeding infected snails to laboratory-reared rats. A natural described by Lie and Umathevy (1965). The first intermediate infection was found in the cattle egret, Bubulcus ibis (Lin- host is the , Lymnaea rubiginosa (Michelin). naeus, 1758). The same and other freshwater snails such as Gyraulus con- The biology of Echinoparyphium (Trematoda) 203

vexiusculus (Hutton), exustus (Deshayes), and niatum, whose current position in the genus Echinoparyphium Bellamya ingallsiana (Lea) serve as second intermediate was not supported by the sequence data. Although the ITS data hosts. Adult worms have been obtained under experimental provided insufficient resolution for an unequivocal solution to conditions from pigeons; ducklings; black-headed or chestnut the relationships within the genus Echinostoma, it supported munias, Lonchura ferruginosa (Sparrman); spotted munias, the identification of E. ellisi and the distinct species status of Lonchura punctulata (Linnaeus); and Java sparrows, Padda three isolates of as predicted from the oryzivora (Linnaeus); but not from rats, mice, and hamsters. ND1 data (Kostadinova et al. 2003). Kiseliene and Grabda-Kazubska (1990) described The taxonomic status of two species, Echinostoma revo- E. pseudorecurvatum sp. nov. It differs from E. recurvatum lutum and Echinoparyphium recurvatum, which commonly sensu stricto at all stages of the life cycle. The most marked infect poultry and other birds, as well as human, is problem- differences occur in the cercariae and relate to the structure of atical. Previous phylogenetic analyses of Southeast Asian the tegument, length of oesophagus, number of flame cells, strains indicate that these species cluster as sister taxa. The and chaetotaxy. Adults differ by body armature, including first internal transcribed spacer (ITS1) sequence was used by shape and size of collar spines. Planorbis planorbis is the first Saijuntha et al. (2011a) for genetic characterization and to ex- intermediate host, tadpoles and young frogs (as well as snails amine the phylogenetic relationships between an isolate from harboring parthenitae) are the 2nd intermediate hosts; domes- Thailand with other isolates available from GenBank data- tic chickens, ducks and pigeons were experimental final hosts. base. Interspecies differences in ITS1 sequence between Grabda-Kazubska and Kiseliene (1991) described the life E. revolutum and E. recurvatum were detected at 6 (3%) of cycle of E. mordwilkoi in which the prosobranch snails Valvata the 203 alignment positions. Of these, nucleotide deletion at piscinalis served as first and second intermediate hosts and positions 25, 26, and 27, pyrimidine transition at 50, 189, and charadriid birds (wading and shore birds such as plovers and pyrimidine transversion at 118 were observed. Phylogenetic killdeers) as the final hosts. They also showed that cercariae analysis revealed that E. recurvatum from Thailand clustered released from V. piscinalis in Lithuania have morphological as a sister taxa with E. revolutum and not with other members characteristics representative of the E. recurvatum complex; of the genus Echinoparyphium. This result confirms a report these cercariae appeared identical to those of E. mordwilkoi. based on allozyme electrophoresis and mitochondrial DNA Kanev et al. (1994) described the life cycle E. cinctum with that E. revolutum and E. recurvatum in Southeast Asia are sis- lymnaeid snails as first intermediate hosts; snails, frogs and ter species (Saijuntha et al. 2011a). The taxonomic status of turtles as second intermediate hosts; and various birds as de- E. recurvatum in Thailand, as well as in Southeast Asian coun- finitive hosts. The life cycle of E. rubrum (Cort, 1914) comb. tries needs to be confirmed and revised using more compre- n. has been completed experimentally. All of the develop- hensive analyses based on morphology and other molecular mental stages , miracidium, sporocyst, mother and daugh- techniques (Saijuntha et al. 2011b). ter rediae, cercaria, metacercaria, and adult were examined Vodyanitskii et al. (2002) used a portrait-based description and described by Kanev et al. (1998). Tables I and II list some of the life cycle of the trematode E. aconiatum as a model for of the Echinoparyphium spp. found in birds and mammals. a GeneNet database. This database was optimized with regard to annotating information and portrait-based visualization of network interactions in ecosystems in terms of hierarchical Genetic characterization levels. Detwiler et al. (2010, 2012) investigated the systematic is- The Echinoparyphium has a history of systematic revision, sues associated with trematodes of muskrats. For echinos- which can make parasite identification a difficult task. In order tomes, ND1 sequences revealed at least 5 genetic lineages. to investigate the relationships within the Echinostomatidae The ND1 phylogeny demonstrated that the muskrats were in- two data sets of gene sequences were analyzed by Kostadi- fected with 5 echinostome lineages: 3 E. trivolvis lineages, nova et al. (2003). The first consisted of all previously pub- 1 E. revolutum, and 1 Echinoparyphium lineage. lished ND1 sequences (20) together with 17 new sequences. The latter represented six species from the cosmopolitan gen- era Echinostoma, Echinoparyphium, and Isth- Behavioral and biochemical studies miophora. The second data-set of ITS sequences again included all previously published sequences (12) and three Temperature can influence the transmission and establishment new sequences from species of Echinostoma, Echino- of E. recurvatum in L. peregra. For E. recurvatum the chang- paryphium and Isthmiophora. All new isolates, as well as ing photo and geotactic behavior over time (McCarthy 1999, voucher material from five previously sequenced isolates, Morley et al. 2003) will also lead to an accumulation of cer- were identified on the basis of morphological characters. The cariae in different parts of the water column, particularly in phylogenetic trees inferred from the ND1 data set helped to areas associated with potential second intermediate hosts. clarify the generic affiliation of all isolates and confirmed the Field studies by Morley et al. (2010) indicate a gradual accu- morphological identifications. The only exception was E. aco- mulation of metacercariae over the summer. This suggests that 204 Jane E. Huffman and Bernard Fried

at any hourly time period a low cercarial density rather than a of emergence from the cyst wall through the escape aperture, high density is more likely in the aquatic medium. Morley et it is an active process and the media consisted of a pH 2 to 4, al. (2010) studied the emergence of E. recurvatum cercariae reducing conditions, temperatures of 37 to 39°C and presence from L. peregra under natural sunlight conditions, using nat- of sodium cholate. In Stage II, the metacercaria is released from urally infected snails of different sizes (10–17 mm) within a the host: the media requires trypsin (Howell 1970). temperature range of 10–29 C. There was a single photoperi- Fried and Grigo (1975) found that excystation require- odic circadian cycle of emergence with one peak, which cor- ments for E. flexum were less fastidious than those of E. ser- related with the maximum diffuse sunlight irradiation. ratum as described by Howell (1968b, 1970). Fried and Grigo Zbikowska (2011) reviewed the important role of ther- (1975) were able to excyst their species of Echinoparyphium mobehavioral snail reactions in the maintenance of the host- in an alkaline medium of trypsin-bile salts in Earle’s balanced parasite system. Behavioral anapyrexia (reverse process of salt solution at 39°C. There was no need for an acid pretreat- behavioral fever) is not evident from L. stagnalis infected by ment, a reductant, or special gases. Excystation requirements E. aconiatum. All snails (with and without emerging cercariae) vary from one Echinoparyphium species to another. chose the same temperature (over 25°C) as non-infected Muller et al. (1999) provided quantitative data on the neu- L. stagnalis. The aggressive larvae of E. aconiatum may stop tral lipid content of a 45-collar-spined Echinoparyphium sp. defensive adaptive response of the host to benefit rapid de- cercaria from Physa sp. High performance thin-layer chro- velopment of parasite larvae. The lack of this behavior in matographic analysis (HPTLC) was used to determine the snails with emerging E. aconiatum cercariae seems to disad- major neutral lipids in cercariae obtained following snail iso- vantage the host but benefits parasite development and pro- lation. The cercarial lipids were identified as free sterols, free gression through the life cycle. Transmission of E. aconiatum fatty acids, and triacylglycerols. The most abundant fraction cercariae into the second intermediate host is easier at higher (free sterols) was quantified by densitometric HPTLC and the ambient temperatures, because of higher larvae invasiveness, amount of free sterol (mainly cholestrol) was 0.022– and also similar thermal preferences of E. aconiatum infected 0.0021~ng per cercaria. This was the first time that quantita- and non-infected snails increase the chances for encounters tive HPTLC was used to quantify neutral fats in an echino- with potential hosts for the metacercariae (Zbikowski and stome cercaria. The function of neutral lipids in cercariae is Zbikowska, 2009). speculative. Cholesterol is probably an important structural Experimental infection of E. recurvatum cercariae in the constituent of the cells and tissues of the cercaria. Echinos- snail second intermediate host Lymnaea peregra shows that tome cercariae have abundant excretory concretions (calcare- metacercarial encystment takes place on the lining of the man- ous corpuscles) of dubious function and cholesterol may be tle cavity, pericardial cavity and kidney lumen, with the man- associated with these concretions. tle cavity the most preferred site. All three sites are accessible The spatial relationship between the musculature and the via the body openings. The metacercariae appear to be more NADPH-diaphorase (NADPH-d) activity, 5-HT and FMR- susceptible to encapsulation in the visceral mass than in the Famide immunoreactivities in redia, cercaria and adult E. aco- cavity of the mantle, pericardium and the lumen of the kidney niatum was studied using scanning electron microscopy (Adam and Lewis 1992). (SEM), NADPH-d histochemistry, immunocytochemistry, and Voutilainen (2011) investigated whether confocal scanning laser microscopy (CSLM). TRITC-conju- could reduce the production of E. aconiatum cercariae in in- gated phalloidin was used to stain the musculature. Staining fected snails L. stagnalis (: ) without for NADPH-d was observed in the central (CNS) and periph- killing the hosts. Praziquantel is a broad-spectrum anti- eral nervous system (PNS) of all three stages. NADPH-d pos- helminth agent. It caused a total cessation of cercaria shed- itive nerves occurred very close to muscle fibres. 5-HT- ding when the praziquantel concentration in the treatment bath immunoreactive (5-HT-IR) nerve cells and fibres occurred in was 10 mg/L and the treatment time was 30 h or longer. the CNS and PNS and close to muscle fibres. FMRFamide- Howell (1968b) investigated the excystment of E. serra- IR nerve fibres were observed in the CNS and PNS of adult tum metacercariae. The cysts excysted within 10 min in a worms. This is the first time, the presence of the NADPH-d trypsin/sodium cholate solution after successive pretreatments has been demonstrated in the larval as well as the adult stages with pepsin and sodium dithionite. Excystment appears to be of a trematode (Terenina et al. 2006). an active process as the cyst wall is unaffected by the treat- ment except in the vicinity of the ‘escape aperture’. Optimum The influence of abiotic and biotic factors on Echino- development to sexual maturity in vivo required 72 h. paryphium and the value of Echinoparyphium as a bioindi- Metacercarial cysts of E. serratum were obtained from the cator of freshwater quality pericardium of the snail Isidorella brazieri. Each cyst was sur- rounded by a nucleated, syncytial host capsule. The cyst wall Aquatic molluscs are ideal invertebrate model systems for en- consisted of 2 layers containing acid and neutral mu- vironmental monitoring and toxicology. Molluscs are sub- copolysaccharide but little or no protein. Excystment of metac- jected to a wide range of infectious diseases that can have ercariae appears to take place in stages. Stage I, which consists significant effects on host ecology and physiology and are The biology of Echinoparyphium (Trematoda) 205

therefore a source of natural stress to populations. Anthro- system in which water temperature acts as a main regulating pogenic activities, especially involving chemical contaminants factor. The three main components of the system interact with that pollute the environment, can also affect molluscan eco- each other and are influenced by various external factors, re- logical and physiological parameters. Pollution and pathogens sulting in a dynamic ecological system (Sankurathri and in combination represent a serious threat to the health of Holmes 1976). aquatic communities. Morley (2010) reviewed the interactive Evans (1982) observed that at concentrations ranging from effects of viral, bacterial, protozoan, and trematode infections 0.1 to 10.0 mg/l, copper and zinc reduced both the longevity with toxic pollutants on aquatic molluscs. and infectivity of E. recurvatum cercariae. Concentrations of Trematodes possess elaborate sensory organs and sophisti- 10.0 mg/l copper and zinc in hard water reduced the time to cated neuromuscular systems. Sukhdeo and Sukhdeo (2004) 50% mortality of cercariae from 30.5 h to 8.5 h and 15.5 h, reviewed the complex patterns of innate behavior of trema- respectively. Copper-induced effects upon cercarial infectivity todes which can be released by specific signals from the envi- were particularly severe and exposures of cercariae to 0.5 mg/l ronment. The evidence in their review suggests that trematode of this metal for as little as 15 min caused significant reduc- parasites live in ecologically predictable aquatic and internal tions in their ability to infect molluscan 2nd intermediate host environments where they perceive only small subsets of hosts. Water hardness had a marked influence on copper tox- the total information available from the environment. A general icity but had a much lower effect on the toxicity of zinc. The conclusion of the review was that host finding in miracidia and results in Evans (1982) laboratory study have also been found cercaria, and site-finding by trematodes migrating within their to occur in polluted, freshwater habitats. definitive hosts, is accomplished through the release of innate Short-term simultaneous effect of high concentrations patterns of behaviors which are adaptive within the context of (LC25, LC50, LC75) of heavy metal ions. (Cu2+, Zn2+, Cd2+ conditions in the worm’s environment. and Pb2+) and infection with trematode partenites Echino- Thieltges et al. (2008) recognized 6 different types of bi- paryphium aconiatum onto haemolymph of molluscs was in- otic factors with the potential to alter larval transmission vestigated by Kirichuk (2002). He reported that low doses of processes which are underestimated determinants in the trans- toxicant (2.5 and 10 maximum admitted concentrations) have mission ecology of free-living trematode stages. These effects variable effects. In infected molluscs the concentration of he- are likely to interact with natural abiotic factors: pH, temper- moglobin decreases, while in intact ones it increases. ature, salinity, water hardness, UV-radiation and anthro- The effect of three ferric chloride concentrations (100, 200, pogenic pollutants. 300 mg/l) on the acid-alkaline balance of haemolymph and In freshwater systems, non-point source pollution affects haemoglobin content in Planorbarius corneus under normal the physical characteristics of the habitat and the endemic bi- conditions and in the case of infection with parthenites and otic assemblages. Free living miracidial and cercarial larval larvae of Echinoparyphium aconiatum was examined by Stad- stages will exhibit graded responses to various types of dis- nichenko et al. (2001). In the medium with an effective con- turbances and may be used as indicators of habitat conditions. centration of ferric chloride, all snail specimens proved to Environmental stressors have the potential to greatly impact have acidified haemolymph, by 40–50% in infected samples the transmission of parasites with complex, multi-host life cy- and 80–85% in uninfected ones. Statistically reliable differ- cles such as those of trematodes. The effects of heavy metal ences in the haemoglobin content in the haemolymph of in- toxicity on host–parasite interactions in freshwater snails have fected and uninfected specimens between the control and test been the subject of several investigations. Metal-induced media were absent, that proves a weak toxic effect of ferric changes in host survival (Guth et al. 1977, Stadnichenko et al. ions on P. corneus. 1995), cercarial emergence, and the physiochemical proper- Stadnichenko and Kirichuk (2002) investigated the com- ties of host hemolymph have been studied in both naturally bined effect of the trematode infection (Echinoparyphium sp.) and experimentally infected snails. and various concentrations of chromium sulphate (0.01, 1, 100 Sankurathri and Holmes (1976) reported on the effects of mg/l) onto the crude protein content in the haemolymph of the thermal effluents on the dynamics of larval helminth parasites mollusc Viviparus viviparous. Under the low intensity of the and on populations of chaetogasters harbored by Physa gy- trematode infection, the contents of crude protein in the rina. Thermal effluents provided the necessary conditions to haemolymph remains normal, while in the case of heavy in- maintain digenean parasite transmission throughout the year fection, it decrease 100 times or lower. In the cases of 0.01–1 between definitive and intermediate hosts, and increased the mg/l concentrations of chromium sulphate, the content of pro- prevalence of certain parasites, especially the metacercarial tein in the haemolymph of V. viviparus decreases, while in the stages. Under experimental conditions the number of E. re- case of 100 mg/l it increases abruptly, in comparison to the curvatum larvae penetrated Physa gyrina was inversely re- norm. The trematode infection intensifies these processes. lated to the number of C. l. limnaei present. It was also The toxicity of cadmium, zinc and Cd/Zn mixtures to the observed that these oligochaetes actively ingested digenean transmission of E. recurvatum cercariae into the snail second larvae. Elimination of C. l. limnaei caused by thermal effluents intermediate hosts was investigated at concentrations ranging has augmented the metacercarial infections. This is a complex from 100 microg l–1 to 10 000 microg l–1 in both soft and 206 Jane E. Huffman and Bernard Fried

hard water by Morley et al. (2002). A differential response in mug 1-1 Cd for 72 h caused a significant increase in the inci- the infectivity of metal-exposed cercariae into Lymnaea pere- dence of first host encystment when compared to controls. In gra and Physa fontinalis was demonstrated which was de- addition, autometallographic staining of E. recurvatum daugh- pendent on the snail species being infected. Exposure of ter rediae and developing cercariae showed that there was L. peregra, P. fontinalis and L. stagnalis to heavy metals metal accumulation within their body tissues. caused a differing susceptibility to E. recurvatum cercariae de- Morley et al. (2006) reviewed the effects of pollutants on pending on the snail species being exposed. the immunology and physiology in both vertebrate and mol- Morley et al. (2003) investigated the toxicity of cadmium luscan host-trematode systems and the implications for para- to a population of Lymnaea peregra and L. stagnalis naturally site transmission. The combined stress induced by pollution infected with a range of digeneans and collected from a num- and parasitism influences the physiology of the host which ber of sites in the lower Thames Valley, UK. Lymnaeid snails can have implications not only on host survival but also on were exposed to 100 microg l–1 cadmium and the effects on the functional biology of resident parasite populations. host survival and emergence of cercariae recorded. Overwin- The commonly used herbicide atrazine has been shown to tered L. peregra, but not L. stagnalis, showed significantly re- affect the susceptibility of second intermediate hosts (such as duced survival compared to seasonally infected snails, i.e. larval ) to trematode infection, as well as the snails which have acquired an infection during the spring or longevity and infectivity of the free-swimming cercariae, but summer. A significant increase in survival with increasing not eggs or the free-swimming miracidia that infect the gas- snail size was demonstrated for L. stagnalis and for seasonally tropod first intermediate hosts (Koprivnikar and Walker 2011). infected L. peregra only. Only L. stagnalis infected with Koprivnikar and Walker (2011) reported that a concentration Diplostomum spathaceum and L. peregra infected individu- of 0.33 µg/L of an atrazine metabolite, desethyl atrazine, in- ally with D. spathaceum, Sanguinicola inermis, E. recurva- creased the mortality of freshwater gastropods (Stagnicola tum and Notocotylus attenuatus demonstrated a significantly elodes) infected with a gymnocephalus type of cercaria but reduced survival compared to laboratory-bred controls. Cad- not that of uninfected snails or those harboring a mature or mium-exposed L. peregra showed no difference in the emer- dormant infection of Echinoparyphium sp. In contrast, 2 wk of gence of E. recurvatum cercariae over a 3-day exposure exposure to desethyl atrazine did not affect the emergence of period. In this study, the toxicity of cadmium to a population gymnocephalus cercariae from snails, although a trend for a of Lymnaea sp. naturally infected with several species of di- decrease in the emergence of Echinoparyphium sp. cercariae geneans, demonstrated several interesting points. The differ- was observed. The combination of simultaneous trematode in- ent susceptibility of overwintered L. peregra and L. stagnalis fection and exposure to contaminants may represent a signif- to cadmium may be species-specific and may reflect either the icant stress to gastropods. The response to the herbicide may ‘health’ of the host species or the environmental conditions in likely be parasite species-specific as well as dependent on which hibernation took place. The increased survival of whether cercariae are being actively produced. L. stagnalis with increased snail size may be due to the larger specimens being more efficient at binding cadmium to metal- Pathology of Echinoparyphium lothioneins and other low-molecular weight proteins, or to a longer time required for cadmium uptake, or to an increased Histological observations of B. truncatus naturally infected by resistance to unfavorable environmental conditions due to a both S. bovis and E elegans in Sardinia, , have shown that superior ability of larger snails to aestivate (Godan 1983). E. elegans is pathogenic to the mollusc and dominant to the Morley et al. (2004a) investigated the toxicity of the anti- schistosome. E. elegans rediae and metacercariae acted by ex- fouling biocides tributyltin (TBTO), copper, and Irgarol 1051 erting pressure on host tissues; rediae, mainly young and (irgarol) at a nominal concentration of 10 μg/l against the vi- motile ones, also behaved as predators. The organs of the mol- ability of E.recurvatum metacercarial cysts within two com- lusc were affected to varying degrees; the ovotestis totally dis- mon freshwater snails, Lymnaea peregra and Physa fontinalis. appeared. The larval development of S. bovis was disturbed; Reduced parasite viability was found under most exposures cercariogenesis was strongly inhibited and gave way to high in both snail species. However a greater effect of toxicant ex- sporocystogenesis. The intensity of this interference depended posure was found in cysts within P. fontinalis compared to on the density of the echinostome larvae present (Mouahid those in L.peregra. This was associated with an increased mor- and Mone, 1990). tality of the host snail. Among all tested biocides, TBTO ex- During the patent period, E. aconiatum cercariae abandon posures induced the highest mortality to both the parasite and the host by breaking through the body wall of the snail. This their hosts. These results suggest that parasite viability is in- process can be very harmful for the host, because of the large terlinked with survival of the host snail. size of the parasitic larvae (body: 521 × 198 µm; tail: 687 × 83 The effect of cadmium exposure of the snail first interme- µm) ( Zbikowski and Zbikowska 2009). Cercariae actively diate host Lymnaea peregra on the incidence of encystment swim toward different pulmonate or prosobranch snails. Non- of E. recurvatum cercariae without emergence from the snail infected individuals are the best hosts for metacercariae, be- was investigated by Morley et al. (2004b). Exposure to 100 cause a parasitized first intermediate host shows increased The biology of Echinoparyphium (Trematoda) 207

mortality upon cercariae repenetration (Lim and Heyneman aspects of infection with Echinoparyphium need more clarifi- 1972). cation. Differential diagnosis by fecal examination is difficult Zbikowska and Zbikowski (2005) observed differences because of morphological similarity of eggs. Praziquantel is between shell shapes of naturally E. aconiatum infected effective for most intestinal fluke infections. Continued efforts snails and non-infected snails. These authors noticed that to understand epidemiological significance of intestinal fluke the youngest whorl of shells E. aconiatum infected L. stag- infections, with detection of further human cases, are required nalis was more slender than the corresponding youngest (Chai et al. 2009). shell whorl of non-infected snails. Echinoparyphium aco- niatum castrates the snail host by direct ingestion of host tissues ( Zbikowska 2006). E. aconiatum castrate their host- References snail. The rediae of E. aconiatum ingest and consume snail tissue, and their large size likely divert host reproductive Adam M.E., Lewis J.W. 1992. Sites of encystment by the metacer- cariae of Echinoparyphium recurvatum in Lymnaea peregra. energy and utilize it for their own development. Zbikowska Journal of Helminthology, 66, 96–99. DOI: 10.1017/S0022 (2011) reported that E. aconiatum infected snails (active and 149X00012657. wintering hosts) had higher hemocyte concentration than Ahmad F., Chishti M.Z. 1997. Avian Trematode Parasites of Kashmir. non-infected ones. This was likely in reaction to extensive Part III. Genus Echinoparyphium Dietz, 1909. Oriental Sci- parasite-caused damage to host tissues. Kechemir (1980) re- ence, 2, 41–48. Alishauskaite V.K. 1960. Study of the life-cycle of Echinoparyphium ported that E. combesi provokes castration in the interme- aconiatum Dietz, 1909 (Echinostomatidae). Tezisy Dokladov diate host. Nauchnoj Konferencii Vsesoyuznogo Obshchestva Gelmintol- Kublickiene and Ciuniene (1973) infected ducks with ogov, pp. 15–20. E. recurvatum. Between 3 and 14 days postinfection, intes- Angel L.M. 1967. The life-cycle of Echinoparyphium hydromyos sp. tinal changes such as hyperemia, hemorrhagia, desquamation, nov. (: Echinostomatidae) from the Australian water- rat. Parasitology, 57, 19–30. DOI: 10.1017/S00311820000 and necrosis occurred. Between 14 and 38 days postinfection, 71869. necrotic lesions were found in the duodenum along with Appleton C.C., Donnelly D.M., Eriksson I.M. 1983. The life-cycle desquamation of the mucosa of the ileum and necrotic changes and seasonal abundance of Echinoparyphium montgomeriana in the rectal mucosa. n. sp. (Trematoda: Echinostomatidae) in Natal, South Africa. Echinoparyphium recurvatum caused thickening of the South African Journal of Zoology, 18, 320–325. Azim M.A. 1930. On the identification and life history of Echinos- serosal surface of intestinal wall. Catarrhal inflammation was toma recurvatum von Linstow, 1873. Annals of Tropical Med- observed on the mucosal surface with many anchored para- icine and Parasitology, 24, 189–192. sites. Bhowmik and Roy (1987) observed severe enteritis in Barker F.D. 1915. Parasites of the American muskrat (Fiber zibethi- turkeys due to E. recurvatum. The spiny head collar and scaly cus). Journal of Parasitology, 1, 184–197. DOI: 10.2307/32 cuticle (Soulsby 1982) of E. recurvatum allow the parasite to 22011. Barker F.D. 1916. A new monostome trematode parasitic in the firmly attached to the site and initiate an inflammatory re- muskrat with a key to the parasites of the American muskrat. sponse (Yousuf et al. 2009). Transactions of the American Microscopical Society, 35, 175– Matta (1980) reported that in chickens infected with As- 184. DOI: 10.2307/3270807. caridia galli, there was little change in the amount of acid Bhowmik M.K., Roy M.M. 1987. Enteric diseases in ducks (Anas phosphatase in the intestine but the alkaline phosphatase was platyrhynchos domesticus). Indian Veterinary Medical Jour- nal, 11, 209–214. increased around the parasites and in the damaged tissues. It Borgsteede F.H.M., Okulewicz A., Zoun P.E.F., Okulewicz J. was reduced when the parasites matured. In Echinoparyphium 2003.The helminth fauna of birds of prey (Accipitriformes, infection the alkaline phosphatase was increased at the sites of Falconiformes and Strigiformes) in the Netherlands. Acta attachment but the acid phosphatase was unchanged. Nath Parasitologica, 48, 200–207. (1977) described the pathology of E. flexum infection in ex- Buscher H.N. 1978. Echinoparyphium speotyto sp. n. (Trematoda: echinostomatidae) from the burrowing owl in Oklahoma, with perimental white leghorn chicks. a discussion of the genus Echinoparyphium. Journal of Para- In Southeast Asia, a total of 59 species of foodborne in- sitology, 64, 52–58. DOI: 10.2307/3279609. testinal flukes have been known to occur in humans. The Canaris A.G., Kinsella J.M. 2000. Helminth parasites in six species largest group is the family Heterophyidae. The next is the fam- of shorebirds (Charadrii) from Bristol Bay, Alaska, U.S.A. ily Echinostomatidae, which includes Echinoparyphium. Var- Comparative Parasitology, 67, 250–252. Chai J.Y., Shin E.H., Lee S.H., Rim H. J., Chai A.F., Shin J.-Y., Lee ious types of are sources of human infections. They E.-H., Rim S.-H., Han-Jong T.I. 2009. Foodborne intestinal include freshwater fish, brackish water fish, fresh water snails, flukes in Southeast Asia. South Korean Journal of Parasitol- brackish water snails (including the oyster), amphibians, ter- ogy, 47, S69–S102. restrial snakes, aquatic insects, and aquatic plants. The reser- Chishti M.Z., Tanveer S. 1992. On a new species of trematode genus voir hosts include various species of mammals or birds. The Echinoparyphium Dietz, 1909 from domestic fowl in Kash- mir. Indian Journal of Parasitology, 16,155–157. host-parasite relationships have been studied for a few species Dar R.L., Ahmad F. 1992. A new record of Echinoparyphium cleric however, the pathogenicity of each parasite species and host Skrjabin (1915) from Anas platyrhynchos in Kashmir. Indian mucosal defense mechanisms are poorly understood. Clinical Journal of Helminthology, 44, 93–96. 208 Jane E. Huffman and Bernard Fried

Dar R.L., Kharo Y.K. 1991. Trematodes of aquatic and migratory birds Ivanov V.M., Semenova N.N. 2000. Parasitological consequences of in Kashmir. Trudy Gel mintologicheskoi Laboratorii, 38, 28–32. introduction. Russian Journal of Ecology 31, 281–283. Davidson W. R., Doster G.L., Pursglove, Jr. S.R., Prestwood A.K. DOI: 10.1023/A:1026687608978. 1977. Helminth parasites of ruffed grouse (Bonasa umbellus) Kanev I., Sorensen R., Sterner M., Cole R., Fried B. 1998. The iden- from the eastern United States. Proceedings of the Helmintho- tification and characteristics of Echinoparyphium rubrum logical Society of Washington, 44, 156–161. (Cort, 1914) new comb. (Trematoda, Echinostomatidae) based Detwiler J.T., Bos, D.H., Minchella D.J. 2010. Revealing the secret on experimental evidence of the life cycle. Acta Parasitolo- lives of cryptic species: Examining the phylogenetic relation- gica 43, 181–188. ships of echinostome parasites in North America. Molecular Kanev I., Radev V., Vassilev I., Dimitrov V., Minchella D. 1994. The Phylogenetics and Evolution, 55, 611–620. DOI: 10.1016/j. life cycle of Echinoparyphium cinctum (Rudolphi 1803) ympev.2010.01.004. (Trematoda: Echinostomatidae) with reexamination and iden- Detwiler J.T., Zajac A.M., Minchella D.J., Belden L.K. 2012. Re- tification of its allied species from Europe and Asia. vealing cryptic parasite diversity in a definitive host: echi- Helminthologia 31, 73–82. nostomes in muskrats. Journal of Parasitology, in press. Kanev I., Sorensen R., Sterner M., Cole R., Fried B. 1992. The iden- Diaz Diaz T. 1976. Studies on life cycles of digenetic trematodes. tification and characteristics of Echinoparyphium rubrum PhD Thesis, University of Leeds, Leeds, West Yorkshire UK. (Cort, 1914) comb. New (Trematoda, Echinostomatidae) Evans N.A. 1982. Effect of copper and zinc upon the survival and based on experimental evidence of the life cycle. Acta Para- infectivity of Echinoparyphium recurvatum cercariae. Para- sitologica, 43,181–188. sitology, 85, 295–303. DOI: 10.1017/S003118200005527X. Kanev I. 1990. A checklist of the helminth parasites of Echinis, Echi- Fain A., Galal A. 1977. Identification of the trematode Echino– nostoma, Echinostomatidae (Trematoda) with references for paryphium recurvatum (von Linstow, 1873) in man and in a thir renaming, replacement and reclassify. Publishing House rodent from Egypt. Annales de la Societe belge de medicine of the Bulgarian Academy of Sciences, Sofia. tropicale, 57, 583–587. Kechemir N. 1980. Description and life cycle of Echinoparyphium Faltýnková A., Našincová V., Kablasková L. 2008. Larval trematodes combesi n.sp. in Bulinus truncates, vector of Schistosoma (Digenea) of the great pond snail, (L.), haematobium in Algeria. Annales de Parasitologie Humaine (Gastropoda: ) in Central Europe: a survey of et Comparee, 55, 57–68. species and key to their identification. Systematic Parasitol- King P.H., Van As J.G. 1996. A description of the life stages of ogy, 69,155–178. DOI: 10.1007/s11230-007-9127-1. Echinoparyphium elegans (Trematoda: Echinostomatidae). Fredensborg B.L., Latham A.D., Poulin R. 2004. New records of gas- South African Journal of Zoology, 31, 145–153. trointestinal helminths from the red-billed gull (Larus novae- Kirichuk G.E. 2002. Effect of different concentrations of heavy metal hollandiae scopulinus). New Zealand Journal of Zoology, 31, ions on the normal physical and chemical characteristics of 75–80. DOI: 10.1080/03014223.2004.9518362. the hemolymph of Palanorbarius purpura (: Bulin- Fried B. 2001. Biology of echinostomes except Echinostoma. Ad- idae) in the norm and during a trematode infection. Parazi- vances in Parasitology, 49, 163–210. DOI: 10.1016/S0065- tologiya, 36, 108–116. 308X(01)49040-3. Kiseliene V., Grabda-Kazubska B. 1990. Echinoparyphium pseudore- Fried B., Graczyk T. 2000. Echinostomes as experimental models for curvatum sp. n. (Trematoda; Echinostomatidae) and its life biological research. Kluwer Academic Publishers, Dordrecht, cycle. Acta Parasitologica Polonica, 35, 285–295. Netherlands, 273 p. Koprivnikar J., Walker P.A. 2011. Effects of the herbicide atrazine’s Fried B., Grigo, K.L. 1975. Infectivity and excystation of the metac- metabolites on host snail mortality and production of trema- ercaria of Echinoparyphium flexum. Proceedings of the Penn- tode cercariae. Journal of Parasitology, 97, 822–827. DOI: sylvania Academy of Science 49, 79–81. 10.1645/GE–2814.1. Godan D. 1983. Pest slugs and snails: biology and control. Kostadinova A. 2005. Familiy Echinostomatidae Looss, 1899. In Berlin/New York, Springer-Verlag. Keys to the trematoda, Volume 2, A. Jones, R. A. Bray, and D. Grabda-Kazubska B. Kiseliene V. 1991. The life cycle of Echino- I. Gibson (eds.). CAB International and Natural History Mu- paryphium mordwilkoi Skrjabin, 1914 (Trematoda: Echinos- seum, London, U.K., p. 9–51. tomatidae). Acta Parasitologica Polonica, 36,167–173. Kostadinova A., Gibson D.I. 2000. The systematics of the Echinos- Guth D.J., Blankespoor H.D., Cairns J. 1977. Potentiation of zinc tomatidae. In Echinostomes as experimental models for bio- stress caused by parasitic infection of snails. Hydrobiologia, logical research, B. Fried, and T. Graczyk (eds.). Kluwer 55, 225–229. DOI: 10.1007/BF00017554. Academic Publishers, Dordrecht, Netherlands, p. 31–57. Harper W.F. 1929. On the structure and life histories of British fresh- Kostadinova A., Herniou E.A., Barrett J., Littlewood D.T. 2003. Phy- water trematodes. Parasitology, 21, 189–219. DOI: 10.1017/ logenetic relationships of Echinostoma Rudolphi, 1809 (Di- S0031182000022897. genea: Echinostomatidae) and related genera re-assessed via Hosseini S.H., Saifuri P., Eslami A., Nabieian S. 2001. Parasitic in- DNA and morphological analyses. Systematic Parasitology fections of gray lag goose (Anser anser) in Gilan province, 54, 159–176. Iran. Journal of the Faculty of Veterinary Medicine, Univer- Kublickiene O., Ciuniene, E. 1973. Histological changes in the mu- sity of Tehran, 56, 56–60. cous membrane of duck intestine during experimental echi- Howell M.J. 1968a. Excystment and in vitro cultivation of Echino- nostomatidosis. Acta Parasitologica Lituanica 11, 73–80. paryphium serratum. Parasitology, 58, 583–587. DOI: Latham, A.D.M., Poulin R. 2002. New records of gastrointestinal 10.1017/S0031182000028882. helminthes from the southern black-backed gull (Larus do- Howell M.J. 1968b. The life-cycle of Echinoparyphium serratum minicanus) in New Zealand. New England Journal of Zo- sp.nov. (Digenea: Echinostomatidae). Parasitology, 58, 573– ology, 29, 253–257. DOI: 10.1080/03014223.2002.9518 582. DOI: 10.1017/S0031182000028870. 309. Howell M.J. 1970. Excystment of the metacercariae of Echino- Lee S.H., Sohn W.M., Chai J.Y. 1990. Echinostoma revolutum and paryphium serratum (Trematoda: Echinostomatidae). Jour- Echinoparyphium recurvatum recovered from house rats in nal of Helminthology, 44, 35–56. DOI: 10.1017/S002214 Yangyang-gun, Kangwon-do. Korean Journal of Parasitol- 9X00021428. ogy, 28, 235–240. DOI: 10.3347/kjp.1990.28.4.235. The biology of Echinoparyphium (Trematoda) 209

Lie K.J., Heyneman D., Jeyarasasingham U., Mansour N., Lee H.F., Morley N.J., Leung K.M.Y, Morrit D., Crane M. 2004a. Toxicity Lee H. 1975. The life cycle of Echinoparyphium ralphaudyi of anti-fouling biocides to encysted metacercariae of Echino- sp. n. (Trematoda: Echinostomatidae). Journal of Parasitol- paryphium recurvatum (Digenea: Echinostomatidae) and ogy, 61, 59–65. DOI: 10.2307/3279107. their snail hosts. Chemosphere, 56, 353–358. DOI: 10.1016/ Lie K.J., Umathevy T. 1965. Studies on Echinostomatidae (Trema- j.chemosphere.2004.01.009. toda) in Malaya. X. The life history of Echinoparyphium Morley N.J., Crane M., Lewis J.W. 2004b. Inence of cadmium ex- dunni sp. n. Journal of Parasitology, 51, 793–799. DOI: posure on the incidence of first intermediate host encystment 10.2307/3276160. by Echinoparyphium recurvatum cercariae in Lymnaea pere- Lim H.K., Heyneman, D. 1972. Intramolluscan inter-trematode an- gra. Journal of Helminthology, 78, 329–332. tagonism: a review of factors influencing the host-parasite Morley N.J., Crane M., Lewis J. W. 2003. Cadmium toxicity and system and its possible role in biological control. Advances snail-digenean interactions in a population of Lymnaea spp. in Parasitolology, 10, 191–268. DOI: 10.1016/S0065-308X Journal of Helminthology, 77, 49–55. (08)60175-X. Morley N.J., Crane M., Lewis J.W. 2002. Toxic effects of cadmium Macko K. J., Špakulová M., Macková A. 2009. Echinoparyphium and zinc on the transmission of Echinoparyphium recurvatum limosorum n. sp. (Trematoda: Echinostomatidae) from Black- cercariae. Journal of Helminthology, 76, 157–163. tailed Godwit, Limosa limosa (Aves, Charadriiformes) in Slo- Mouahid A., Mone H. 1990. Interference of Echinoparyphium ele- vakia. Helminthologia, 46, 220–224. DOI: 10.2478/s11687- gans with the host-parasite system Bulinus truncatus-Schis- 009-0041-8. tosoma bovis in natural conditions. Annals of Tropical Macko K.J., Hanzelova V., Mackova A. 2004. Platyhelminthes of Medicine and Parasitology, 84, 341–348. three species of shorebirds (Charadriiformes) in the Slovak Mouahid A., Mone H. 1988. Echinoparyphium elegans (Looss, 1899) Republic. Helminthologia, 41, 151–159. (Digenea: Echinostomatidae): the life cycle and redescription Mathias P. 1927. Cycle evolutif d’un Trematode de la famille des of the adult with a revision of the 43-spined members of Echiostomidae (Echinoparyphium recurvatum Linstow). An- the genus Echinoparyphium. Systematic Parasitology, 12, nales Des Sciences Naturelles Comprenant la Zoologie, 10, 149–157. 289–309. Mulder E., Smales L.R. 2006. Dusky rat, Rattus colletti (Muridae), Matta S.C. 1980. A note on some histochemical changes in the small a new host for Echinoparyphium hydromyos (Trematoda: Di- intestine of chicks, experimentally infected with Ascaridia genea) in the Northern Territory, Australia. Comparative Par- galli and Echinoparyphium sp. Veterinary Research Journal, asitology, 73, 289–290. 3, 5–56. Muller E.E., Fried B., Sherma, J. 1999. HPTLC determination of neu- McCarthy A.M. 2011. Scanning electron microscopy of adult tral lipids in the cercariae of Echinostoma trivolvis and Echinoparyphium recurvatum (Von Linstow, 1873) (Digenea: Echinoparyphium sp. (Trematoda). Journal of Planar Chro- Echinostomatidae) from Britain. Journal of Helminthology, matography – Modern TLC, 12, 306–308. 85, 453–457. DOI: 10.1017/S0022149X10000787. Najarian H.H. 1954. Developmental stages in the life cycle of McCarthy A.M. 1999. Phototactic responses of the cercaria of Echinoparyphium flexum (linton, 1892) dietz, 1910 (trema- Echinoparyphium recurvatum during phases of sub-maximal toda: Echinostomatidae). Journal of Morphology, 94, 165– and maximal infectivity. Journal of Helminthology, 73, 63– 197. 65. DOI: 10.1017/S0022149X99000086. Najarian H.H. 1953. The Life History of Echinoparyphium flexum McCarthy A.M. 1990. Speciation of echinostomes; evidence for the (Linton 1892) (Dietz 1910) (Trematoda: Echinostomidae). existence of two sympatric sibling species in the complex Science, 117, 564–565. Echinoparyphium recurvatum Von Linstow, 1873 (Digenea: Nath D. 1977. A note on the pathology of Echinoparyphium flexum Echinostomatidae). Parasitology, 101, 35–42. DOI: 10.1017/ (Linton, 1892) Dietz, 1910 infection in experimental white S0031182000079725. leghorn chicks. Indian Journal of Animal Sciences, 45, McCoy O.R. 1928. Life histories on trematodes from Missouri. Jour- 505–507. nal of Parasitology, 14, 207–280. DOI: 10.2307/3271380. Nevostrueva L.S. 1953. The life-cycle of a new echinostomatid of McJunkin J.W., Applegate R.D., Zelmer D.A. 2003. Enteric domestic birds, Echinoparyphium petrowi n.sp. Papers on helminths of juvenile and adult wild turkeys (Meleagris gal- helminthology presented to academician K. I. Skryabin on his lopavo) in eastern Kansas. Avian Diseases, 47, 1481–1485. 75th birthday. pp. 436–439. DOI: 10.1637/7055. Pence D. B., Young V.E., Guthery F.S. 1980. Helminths of the ring- Meyer M.C., Reilly J.R. 1950. Parasites of muskrats in Maine. Amer- necked pheasant, Phasianus colchicus (Gmelin) (Phasianidae) ican Midland Naturalist, 44, 467–477. DOI: 10.2307/ from the Texas Panhandle. Proceedings of the Helmintholol- 2421967. gical Society of Washington, 47, 144–147. Moema E.B.E. 2011. PhD Thesis University of Limpopo Medunsa, Poonswad P., Chatikavanij P. 1989. Echinoparyphium oscitansi n. South Africa. sp. (Trematoda: Echinostomatidae): Natural infection in Asian Morley N.J. 2010. Interactive effects of infectious diseases and pol- open-billed storks (Anastomus oscitans; Aves: Ciconiidae) in lution in aquatic mollusks. Aquatic Toxicology, 96, 27–36. Thailand. Journal of the Science Society of Thailand, 15, DOI: 10.1016/j.aquatox.2009.09.017. 293–299. Morley N.J., Adam M.E., Lewis J.W. 2010. The effects of host size Rausch R. L., Fay F.H., Williamson F.S.L. 1983. Helminths of the and temperature on the emergence of Echinoparyphium re- arctic fox, Alopex lagopus (L.), in Greenland. Canadian Jour- curvatum cercariae from Lymnaea peregra under natural light nal of Zoology, 61, 1847–1851. conditions. Journal of Helminthology, 84, 317–326. DOI: Riech F. 1927. Beitrage zur kenntnis der Echinostomiden. I. Der 10.1017/S0022149X09990666. Lebenaszyklus von Echinoparyphium recurvatum Dtz. II. Morley N.J., Lewis J.W., Hoole D. 2006. Pollutant-induced effects on Cercaria laticaudata n. sp. Centralbl. Fur Bakt. U. Parasit. immunological and physiological interactions in aquatic host– Originale, 103, 279–290. trematode systems: implications for parasite transmission Saijuntha W., Tantrawatpan C., Sithithawoen P., Andrews R.H., Pet- Journal of Helminthology, 80, 137–149. DOI: 10.1079/JOH ney T.N. 2011 a. Genetic characterization of Echinostoma rev- 2006345. olutum and Echinoparyphium recurvatum (Trematoda: Echino- 210 Jane E. Huffman and Bernard Fried

stomatidae) in Thailand and phylogenetic relationships with Sukhdeo M.V.K., Sukhdeo S.C. 2004. Trematode behaviours and the other isolates inferred by ITS1 sequence. Parasitology Re- perceptual worlds of parasites. Canadian Journal of Zoology, search, 108, 751–755. 82, 292–315. Saijuntha W., Sithithawoen P., Dengue K., Kiatsopit N., Andrews Taft S.J., Suchow K., Vanhorn M. 1993. Helminths from some Min- R.H., Petney T.N. 2011 b. Genetic variation and relationships nesota and Wisconsin raptors. Journal of the Helminthologi- of four species of medically important echinostomes (Trema- cal Society of Washington, 60, 260–263. toda: Echinostomatidae) in South-East Asia. Infection, Ge- Terenina N.B., Tolstenkov O., Fagerholm H-P., Serbina E.A., Vod- netics and Evolution, 11, 375–81. janitskaja S.N., Gustafsson M.K.S. 2006. The spatial rela- Sankurathri C.S., Holmes J.C. 1976. Effects of thermal effluents on tionship between the musculature and the NADPH-diaphorase parasites and commensals of Physa gyrina Say (Mollusca: activity, 5-HT and FMRFamide immunoreactivities in redia, Gastropoda) and their interactions at Lake Wabamun, Alberta. cercaria and adult Echinoparyphium aconiatum (Digenea). Canadian Journal of Zoology, 54, 1742–1753. Tissue Cell, 38, 151–157. Schuster R., Schaffer T., Shimalov T. 2002. The helminth fauna of in- Thieltges D.W., Jensen K.T., Poulini R. 2008. The role of biotic fac- digenous white storks (Ciconia ciconia). Berliner und Munch- tors in the transmission of free-living endohelminth stages. ener Tierarztliche Wochenschrift, 115, 435–439. Parasitology, 135, 407–426. Singh H.S., Kumar Y., Arya P.V., Malti. 2002. Echinoparyphium Toledo R., Esteban J.G., Fried B. 2009. Recent advances in the biol- spinosus sp. nov., a new echinostome from Vanellus spinosus ogy of echinostomes. Advances in Parasitology, 69, 147–204. at Meerut. Journal of Experimental Zoology India, 5, 249– Viozzi G., Flores V., Rauque C. 2005. An ectosymbiotic , 252. Temnocephala chilensis, as second intermediate host for Sitko J. 1998. Trematodes of birds of prey (Falconiformes) in Czech- Echinoparyphium megacirrus (Digenea: Echinostomatidae) Republic. Helminthologia, 35, 131–46. in Patagonia (Argentina). Journal of Parasitology, 91, 229– Sohn W.M., Woo H.C., Hong S.J. 2002. Tegumental ultrastructure of 231. Echinoparyphium recurvatum according to developmental Vodyanitskii S.N., Yurlova N.I., Suslov V.V. 2002. Formal description stages. Korean Journal of Parasitology, 40, 67–73. of the trematode ecoparasitic system on using the genenet data Sohn W.M. 1998. Life history of Echinoparyphium recurvatum format. System Computational Biology BGRS, 214–217. (Trematoda: Echinostomatidae) in Korea. The Korean Journal Voutilainen A. 2011. In vivo efficacy of praziquantel against of Parasitology, 36, 91–98. Echinoparyphium aconiatum (Trematoda: Echinostomatidae) Soulsby E.J.L. 1982. Textbook of Veterinary Clinical Parasitology, parasitizing the great pond snails Lymnaea stagnalis (Gas- Vol. I. Helminths. Blackwell Scientific Publications, Oxford. tropoda: Lymnaeidae). Experimental Parasitology, 129, 72–74. Stadnichenko A.P., Kirichuk G.E. 2002. The effect of trematode in- Yousuf M.A., Das P.M., Anisuzzaman M., Banowary B. 2009. Gas- vasion and chromium sulphate on the crude protein content tro-intestinal helminths of ducks: Some Epidemiologic and in the haemolymph of Viviparus viviparus (Mollusca: Gas- pathologic aspects. Journal of Bangladesh Agricultural Uni- tropoda: Pectinibranchia). Parazitologiia, 36, 240–246. versity, 7. 91–97. Stadnichenko A.P., Ivanenko L.D., Kirichuk G.E., Ianovich L.N. Zbikowska E. 2006. Does the parasitic gigantism of Lymnaea stag- 2001. Effect of iron chloride (III) on hematological status of nalis (L.) individuals naturally parasitized with digenetic lar- the Planorbarius corneus (Mollusca: Gastropoda: Bulinidae) vae exist? Malacologist, 46, 18. in normal snails and during infection with trematode parthen- Zbikowska E. 2011. One snail – three Digenea species, different ites. Parazitologiia, 35, 109–113. strategies in host-parasite interaction. Animal Biology, 61, Stadnichenko A.P., Ivanenko L.D., Gorchenko I.S., Grabinskaya 1–19. O.V., Osadchuk L.A., Sergeichuk S.A. 1995. The effect of dif- Zbikowska E., Zbikowski J. 2005. Differences in shell shape of nat- ferent concentrations of nickel sulphate on the horn snail urally infected Lymnaea stagnalis (L.) individuals as the effect (Mollusca: Bulinidae) infected with the trematode Cotylurus of the activity of digenetic trematode larvae. Journal of Par- cornutus (). Parazitologiya, 29, 112–116. asitology, 91, 1046–1051. Zbikowski J., Zbikowska E. 2009. Invaders of an invader – trema- todes in Potamopyrgus antipodarum in Poland. Journal of In- vertebate. Pathology, 101, 67–70.

(Accepted July 05, 2012)